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Papon, N.

Publications and source records attributed to Papon, N..

6 recordsLinked to original sources

Geissoschizine scaffolding enzymes shape monoterpene indole alkaloid biosynthesis

For decades, medicinal plants have been an invaluable source of therapeutics for human health. Among plant specialized metabolites, monoterpene indole alkaloids (MIAs) display remarkable chemical diversity and potent bioactivities, including anticancer properties. While the biosynthetic pathways leading to major MIAs such as vincristine, vinblastine, and camptothecin have been extensively studied, the mechanisms regulating metabolic flux within these pathways remain poorly understood. Here, we uncover an unexpected regulatory layer in MIA biosynthesis involving medium-chain dehydrogenase/reductase (MDR) proteins. Using a combination of in vitro biochemical assays, pathway reconstitution in planta, protein-protein interaction analyses, and metabolic engineering in yeast, we show that specific MDRs do not function as classical catalysts but instead enhance both the activity and diversify the stereochemical outputs of geissoschizine synthase (GS). These proteins physically interact with GS and strictosidine {beta}-glucosidase (SGD), forming ternary complexes that likely facilitate substrate channeling of reactive intermediates. Importantly, introduction of these MDRs into engineered yeast strains leads to a dramatic increase in the production of geissoschizine, a central MIA precursor. Collectively, our findings reveal a previously unrecognized role for MDR proteins as regulators of metabolic flux and highlight their potential as powerful tools for metabolic engineering of valuable plant natural products.

plant biology↗

Evolution of CYP71D as a driving force of the diversification of monoterpene indole alkaloid biosynthesis

Monoterpene indole alkaloids (MIAs) constitute a vast group of plant natural products synthesized within the Gentianales order. MIAs possess outstanding pharmacological properties that explain their wide use in the treatment of human diseases. These biological activities result from the complex structure of MIAs that originate from intricated biosynthetic pathways involving several enzyme families and notably cytochrome P450s. The early steps of MIA synthesis involve several P450s from the 71 clade, which catalyse the conversion of various reduced strictosidine aglycones into MIAs from the mavacurane, strychnane, akuammilane, sarpagane, and heteroyohimane groups. An extensive study of these P450 distribution in genomic resources reveals that they all belong to a single evolutionary lineage named GAS clade, restricted to the MIA producing Gentianales (Gelsemiaceae and Rauvolfioideae). A related but distinct P450 lineage (named sister GAS clade) was found in non-MIA producing Gentianales and species producing structurally distinct MIAs (Rubiaceae). Functional characterization of 36 members of the GAS clade revealed that these enzymes felt into four main groups of activity depending on substrate acceptance (ex: tetrahydroalstonine, geissoschizine, ajmalicine...) and the nature of the catalyzed reaction (aromatization, cyclisation). These characterizations also lead to the identification of a yohimbane aromatization activity for several of these P450s, increasing the number of MIA scaffolds associated with GAS activity to six. Lastly, the chronology of emergence of these GAS activities was assessed by using ancestral sequence reconstitution, establishing that the initial ancestor of the whole GAS clade exhibits a main alstonine synthase activity. Subsequent gene duplication events, combined with neofunctionalization, facilitated the progressive emergence of eight additional activities, variably distributed among the four GAS subgroups. This comprehensive enzyme characterization establishes the evolutionary trajectory of the GAS clade, demonstrating how its diversification has progressively shaped the chemical diversity of MIAs in Gentianales.

biochemistry↗

Genome-based discovery of pachysiphine synthases in Tabernaemontana elegans

Plant specialized metabolism represents an inexhaustible source of active molecules, some of which have been used in human health for decades. Among these, monoterpene indole alkaloids (MIAs) include a wide range of valuable compounds with anticancer, antihypertensive, or neuroactive properties. This is particularly the case for the pachysiphine derivatives which show interesting antitumor and anti-alzheimer activities but accumulate at very low levels in several Tabernaemontana species. Unfortunately, genome data in Tabernaemontanaceae are lacking and knowledge on the biogenesis of pachysiphine-related MIAs in planta remains scarce, limiting the prospects for biotechnological supply of many pachysiphine-derived biopharmaceuticals. Here, we report a raw version of the toad tree (Tabernaemontana elegans) genome sequence. These new genomic resources led to the identification and characterization of a couple of genes encoding cytochrome P450 with pachysiphine synthase activity. Our phylogenomic and docking analyses highlights the different evolutionary processes that have been recruited to epoxidize the pachysiphine precursor tabersonine at a specific position and in a dedicated orientation, thus enriching our understanding of the diversification and speciation of the MIA metabolism in plants. These gene discoveries also allowed us to engineer the synthesis of MIAs in yeast through the combinatorial association of metabolic enzymes resulting in the tailor-made synthesis of non-natural MIAs. Overall, this work represents a step forward for the future supply of pachysiphine-derived drugs by microbial cell factories. Significance StatementWhile pachysiphine is a monoterpene indole alkaloid of high interest and the precursor of an anti-Alzheimer compound, its biosynthesis involving the epoxidation of tabersonine remains uncharacterized. By sequencing and assembling the genome of Tabernaemontana elegans, we identified two P450s exhibiting a pachysiphine synthase activity that we modelized to explore the evolutionary scenario leading to the acquisition of this expoxidase activity; and used to engineer yeast cell factories for securing pachysiphine supply and producing new-to-nature alkaloids.

plant biology↗

All families of transposable elements were active in the recent wheat genome evolution and polyploidy had no impact on their activity

AO_SCPLOWBSTRACTC_SCPLOWBread wheat (Triticum aestivum L.) is a major crop and its genome is one of the largest ever assembled at reference-quality level. It is 15 Gb, hexaploid, with 85% of transposable elements (TEs). Wheat genetic diversity was mainly focused on genes and little is known about the extent of genomic variability affecting TEs, transposition rate, and the impact of polyploidy. Multiple chromosome-scale assemblies are now available for bread wheat and for its tetraploid and diploid wild relatives. In this study, we computed base pair-resolved, gene-anchored, whole genome alignments of A, B, and D lineages at different ploidy levels in order to estimate the variability that affects the TE space. We used assembled genomes of 13 T. aestivum cultivars (6x=AABBDD), T. durum (4x=AABB), T. dicoccoides (4x=AABB), T. urartu (2x=AA), and Aegilops tauschii (2x=DD). We show that 5 to 34% of the TE fraction is variable, depending on the species divergence. Between 400 and 13,000 novel TE insertions per subgenome were detected. We found lineage-specific insertions for nearly all TE families in di- tetra- and hexaploids. No burst of transposition was observed and polyploidization did not trigger any boost of transposition. This study challenges the prevailing idea of wheat TE dynamics and is more in agreement with an equilibrium model of evolution.

genomics↗

Long-read and chromosome-scale assembly of the hexaploid wheat genome achieves higher resolution for research and breeding

The sequencing of the wheat (Triticum aestivum) genome has been a methodological challenge for many years due to its large size (15.5 Gb), repeat content, and hexaploidy. Many initiatives aiming at obtaining a reference genome of cultivar Chinese Spring have been launched in the past years and it was achieved in 2018 as the result of a huge effort to combine short-read sequencing with many other resources. Reference-quality genome assemblies were then produced for other accessions but the rapid evolution of sequencing technologies offers opportunities to reach high-quality standards at lower cost. Here, we report on an optimized procedure based on long-reads produced on the ONT (Oxford Nanopore Technology) PromethION device to assemble the genome of the French bread wheat cultivar Renan. We provide the most contiguous and complete chromosome-scale assembly of a bread wheat genome to date. Coupled with an annotation based on RNA-Seq data, this resource will be valuable for the crop community and will facilitate the rapid selection of agronomically important traits. We also provide a framework to generate high-quality assemblies of complex genomes using ONT.

genomics↗

New insights into homoeologous copy number variations in the hexaploid wheat genome

Bread wheat is an allohexaploid species originating from two successive and recent rounds of hybridization between three diploid species that were very similar in terms of chromosome number, genome size, TE content, gene content and synteny. As a result, it has long been considered that most of the genes were in three pairs of homoeologous copies. However, these so-called triads represent only one half of wheat genes, while the remaining half belong to homoeologous groups with various number of copies across subgenomes. In this study, we examined and compared the distribution, conservation, function, expression and epigenetic profiles of triads with homoeologous groups having undergone a deletion (dyads) or a duplication (tetrads) in one subgenome. We show that dyads and tetrads are mostly located in distal regions and have lower expression level and breadth than triads. Moreover, they are enriched in functions related to adaptation and more associated with the repressive H3K27me3 modification. Altogether, these results suggest that triads mainly correspond to housekeeping genes and are part of the core genome, while dyads and tetrads belong to the Triticeae dispensable genome. In addition, by comparing the different categories of dyads and tetrads, we hypothesize that, unlike most of the allopolyploid species, subgenome dominance and biased fractionation are absent in hexaploid wheat. Differences observed between the three subgenomes are more likely related to two successive and ongoing waves of post-polyploid diploidization, that had impacted A and B more significantly than D, as a result of the evolutionary history of hexaploid wheat. Core ideasOnly one half of hexaploid wheat genes are in triads, i.e. in a 1:1:1 ratio across subgenomes Triads are likely part of the core genome; dyads and tetrads belong to the dispensable genome Subgenome dominance and biased fractionation are absent in hexaploid wheat Subgenome differences are related to two successive waves of post-polyploid diploidization

genomics↗