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Perrot, T.

Publications and source records attributed to Perrot, T..

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↗

A reverse chemical ecology approach to explore wood natural durability

The natural durability of wood species, defined as their inherent resistance to wood-destroying agents is a complex phenomenon depending of many biotic and abiotic factors. Besides the presence of recalcitrant polymers, the presence of compounds with antimicrobial properties is known to be important to explain wood durability. Based on the advancement in our understanding of fungal detoxification systems, a reverse chemical ecology approach was proposed to explore wood natural durability. A set of six glutathione transferases from the white-rot Trametes versicolor was used as targets to test wood extracts from seventeen French Guiana neotropical species. Fluorescent thermal shift assays allowed to quantify interactions between fungal glutathione transferases and these extracts. From these data, a model combining this approach and wood density predicts significantly wood natural durability of the tested species previously estimated by long-term soil bed tests. Overall, our findings confirm that detoxification systems could be used to explore the chemical environment encountered by wood decaying fungi and then wood natural durability.

microbiology↗

A multi-seasonal model of plant-nematode interactions and its use to identify optimal plant resistance deployment strategies

O_LIRoot-knot nematodes (RKNs) are soil-borne polyphagous pests with major impact on crop yield worlwide. Resistant crops efficiently control avirulent RKNs, but favour the emergence of virulent forms. Virulence being associated with fitness costs, susceptible crops counter-select virulent RKNs. In this study we identify optimal rotation strategies between susceptible and resistant crops to control RKNs and maximize crop yield.\nC_LIO_LIWe developed an epidemiological model describing the within-season dynamics of avirulent and virulent RKNs on susceptible or resistant plant root-systems, and their between-season survival. The model was fitted to experimental data and used to predict yield-maximizing rotation strategies, with special attention to the impact of epidemic and genetic parameters.\nC_LIO_LICrop rotations were found to be efficient under realistic parameter ranges. They were characterised by low ratios of resistant plants, and were robust to parameter uncertainty. Rotations provide significant gain over resistant-only strategies, especially under intermediate fitness costs and severe epidemic contexts.\nC_LIO_LISwitching from the current general deployment of resistant crops to custom rotation strategies could not only maintain or increase crop yield, but also preserve the few and valuable R-genes available to us.\nC_LI

ecology↗

A Nature-based solution in practice: ecological and economic modelling shows pollinators outperform agrochemicals in oilseed crop production

AO_SCPLOWBSTRATC_SCPLOWNature-based agriculture, reducing dependency on chemical inputs, requires using ecological principles for sustainable agro-ecosystems, balancing ecology, economics and social justice. There is growing evidence that pollinator-dependent crops with high insect pollination service can give higher yields. However, the interacting effects between insect pollination and agricultural inputs on crop yields and farm economics remain to be established to reconcile food production with biodiversity conservation. We investigated the effects of insect pollination and agricultural inputs on oilseed rape (Brassica napus L.). We show that not only yield but also gross margins are 16-40% higher in fields with higher pollinator abundance than in fields with reduced pollinator abundance. This effect is however strongly reduced by pesticides use. Higher yields may be achieved by either increasing agrochemicals (reducing pests) or increasing bee abundance, but crop economic returns was only increased by the latter, because pesticides did not increase yields while their costs reduced gross margins.

ecology↗