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Petriacq, P.

Publications and source records attributed to Petriacq, P..

16 recordsLinked to original sources

Interspecific transfer of specialized metabolites in root exudates coincides with root chromatin regulation and systemic chemical defenses in rice

O_LIBenzoxazinoids are indole-derived specialized metabolites released into the soil through root exudates. Initially studied for their allelopathic and toxic effects, they are now recognized as broad regulators of plant-organism interactions, including microbiome-mediated pathogen resistance. However, whether benzoxazinoid-containing root exudates can directly influence disease susceptibility in neighboring plants remains unclear. C_LIO_LIUsing an agriculturally relevant rice-maize co-culture system, we show that benzoxazinoids naturally exuded by maize roots are taken up by rice roots and are associated with reduced rice blast disease in leaves. C_LIO_LIThis protection occurs without detectable benzoxazinoid accumulation in rice leaves, constitutive immune activation or decreased plant height. Instead, benzoxazinoid uptake by rice roots is associated with chromatin hyperacetylation, increased expression of key phenylpropanoid biosynthetic genes and broad metabolic reprogramming. C_LIO_LIThese responses extend systemically to leaves, where rice establishes a defense-related chemical state distinct from the systemic acquired resistance previously observed in benzoxazinoid-dependent, microbiome-mediated plant-soil feedbacks. C_LIO_LIOur findings support a model in which specialized metabolites exuded by one crop species are acquired by a neighbouring species and trigger chromatin-associated metabolic reprogramming linked to systemic chemical defence. This study provides a molecular framework connecting plant-plant chemical interactions, root exudation, chromatin regulation and disease susceptibility. C_LI

plant biology↗

Effects of an increase in water temperature on inter- and transgenerational plasticity reveal a short-term metabolic and phenotypic memory in an aquatic plant species

Transgenerational plasticity can shape plant phenotype and influence plant response to environmental changes in interaction with the current conditions. While how past stress interact with either current optimal or stress conditions is increasingly documented within a single plant, transgenerational plasticity remains particularly poorly understood especially at the metabolome level. In our study, we investigated whether heat stress induces transgenerational metabolic and phenotypic modifications along two successive clonal ramet generations of the sub-Antarctic aquatic plant Limosella australis. We performed untargeted metabolomics approaches and measured morphologic and performance traits, to assess both transgenerational plasticity of the metabolome and the phenotype. We found that heat stress remodelled the metabolic profile and influenced the foraging strategy of our clonal plant, and that some of these metabolic changes persisted into the first clonal generation. This one therefore adopted an intermediate growth strategy, even though culture conditions were optimal. By comparing differentially accumulated features between daughter ramets from heat stressed mother ramets and from unstressed mother ramets, we identified common and specific metabolites accumulation to heat stress response, belonging to diverse compound families. However, we did not observe any adaptative advantage and any metabolic imprint during another heat stress applied on the second clonal generation. This work provides especially new clues into how plant metabolome integrates and transfers previous stressed clonal generations information.

plant biology↗

From definition to discovery: metabolite markers of high temperature in green grape berries

Understanding how plants respond to high temperature is critical under global warming. Metabolite markers can provide insights into stress-responsive mechanisms and help guide strategies to maintain crop quality. However, heat-associated metabolite markers in grape berries remain poorly defined, particularly at the green stage, a critical phase of berry development during which early metabolic perturbations can influence subsequent ripening and ultimately determine berry composition and quality. Here, we applied berry-scale heat treatments of eight durations of two major wine cultivars, Cabernet Sauvignon and Merlot. Untargeted LC-MS profiling revealed both conserved and cultivar-dependent responses to heat. Based on these patterns, three time points were selected for targeted GC-MS analysis, and subsequent statistical analyses identified robust "cultivar-common heat markers": glycine decreased, whereas galactinol increased consistently across time points and cultivars. "Cultivar-dependent heat markers" were identified: xylose, lyxose, citrulline, quinic acid, and glutamine, that consistently distinguished CS and Merlot fruits under heat stress. Notably, xylose, lyxose, citrulline, and quinic acid also differentiated the two cultivars under ambient conditions, underscoring their potential as stable cultivar-discriminating metabolites. Together, these results reveal dynamic metabolic remodeling in grape berries under heat stress, particularly in amino acid, nitrogen, central carbon metabolism, raffinose family oligosaccharides pathway and the glutathione-ascorbate cycle.

plant biology↗

Predictive metabolomics to decipher plant eco-evolutive tendencies and physiological traits

Plant ecological and evolutionary strategies are shaped by interactions between phylogenetic history and environmental constraints, resulting in leaf and stomatal traits. However, traditional trait-based and phylogenetic approaches often fail to fully explain biochemical mechanisms underlying ecological strategies, particularly for leaf and stomatal traits. Plant metabolomes integrate genetic, physiological, and environmental information and therefore represent a promising intermediate phenotype for investigating links between biochemical diversity, functional traits, and evolutionary patterns. We analysed metabolomic profiles from 74 plant species with various growth forms and ecological types. Using machine learning approaches, we explored whether metabolic variation could predict plant functional divisions, growth forms and phenological types, but also physiological traits related to drought resistance. Metabolomic data contained structured information associated with variation in plant functional traits, ecological strategies, and phylogenetic relationships. Machine learning models identified with high accuracy distinct metabolic signatures linked to differences among plant functional divisions, growth forms, phenology, and trait values. Our study demonstrates that predictive metabolomics provides a powerful and integrative framework to investigate plant ecological and evolutionary strategies. By linking biochemical diversity with plant phylogeny, and ecophysiological traits across multiple species, this approach offers new opportunities to explore the mechanistic basis of plant evolution.

plant biology↗

Multi-omic analysis of maize NILs for chilling tolerance QTLs uncover regulatory and metabolic signatures

Early sowing of maize (Zea mays L.) is increasingly required to mitigate summer drought under climate change, making the acquisition of chilling tolerance a major agronomic challenge. Here, we investigated the molecular and physiological bases of cold tolerance using two maize near-isogenic lines (NILs) differing at two major chilling tolerance quantitative trait loci (QTLs) located on chromosome 4. Plants were exposed to low temperature (14{degrees}C day/10{degrees}C night) for 20 days and analyzed using an integrated multi-omics approach combining transcriptomics, soluble and cell wall proteomics, and metabolomics (primary and specialized metabolites), together with physiological measurements. Univariate and multivariate analyses revealed significant chilling-induced variability across all molecular layers, affecting [~]0.2% of genes, [~]6% of proteins, and a subset of specialized metabolites, while primary metabolites were largely stable. Integrative statistical analyses demonstrated that the soluble and cell wall proteomes contributed most strongly to the genotype effect, highlighting protein-level regulation as a major determinant of chilling tolerance. A restricted 5.15 Mb divergence region on chromosome 4 was sufficient to drive contrasting physiological responses, including differences in photosynthetic charge separation efficiency and leaf development, favoring the chilling-tolerant NIL. Notably, several components of the benzoxazinoid pathway located within the divergence region, including BX1 and associated specialized metabolites (BZX-like glucoside, DIBOA-glucoside-2, HBOA-glucoside-2), were specifically associated with chilling tolerance, suggesting a role in stress signaling and hormonal crosstalk. Overall, this study demonstrates that integrative multi-omics analyses provide a powerful framework to resolve genotype-specific regulatory mechanisms underlying chilling tolerance in maize and to identify candidate molecular targets for breeding. HighlightsO_LIFirst organ-resolved multi-omics dissection of chilling responses in maize NILs. C_LIO_LIA 5.1Mb divergence on chromosome 4 drives major physiological and molecular differences. C_LIO_LIChilling tolerance is linked to more robust photochemical homeostasis and sustained leaf development. C_LIO_LISoluble and cell-wall proteomes dominate the genotype-discriminating -omics signal. C_LIO_LIBenzoxazinoids and defense-related transcriptional modules are differentially activated. C_LIO_LICell wall remodeling enzymes and apoplastic peroxidases emerge as key tolerance players. C_LI

plant biology↗

Paleometabolomics reveals impacts of abiotic factors on rodent midden metabolism over the last 50,000 years.

Metabolomics and paleoecology combined can reveal how past ecosystems worked, helping us predict future changes more accurately. Pioneering studies are needed to shed light on the potential of the so-called paleometabolomics and to standardise its application. Here, we deployed an untargeted metabolomic workflow on a timeline (200 to 49,600 cal yr BP) of rodent middens that efficiently and reproducibly captured rodent midden metabolic diversity, recovering 79% of the richness detected in 15 contemporary plant species. We found that midden chemical diversity and metabolites were influenced by the midden composition, age, and environment. Variation at the metabolite level in middens could fit age, past temperature and precipitation levels with an R{superscript 2} > 88% and their plant composition. Compounds and families responding to climate variation included lipids (e.g. glycerophospholipids) and other metabolites linked to redox status such as phenolics (e.g. flavonoids, lignans). The responses of significant midden chemical indices and compounds to abiotic pressures were supported by their response in plants collected near the midden sites to temperature and soil water content across an elevation gradient. Overall, our results not only showcase paleometabolomics as a powerful tool to reconstruct past ecosystem dynamics and metabolic evolutionary trajectories, but also to uncover relevant chemical families that could serve as trackers of past -and potentially future- climate fluctuations.

ecology↗

Predictive metabolomics reveals leaf systemic metabolic signatures associated with floral traits in Camellia

The genus Camellia comprises more than 200 evergreen species of major economic and ornamental importance, characterised by high morphological and chemical diversity. While several species have been extensively studied for their bioactive compounds, the metabolic basis of floral trait variation across the genus remains poorly understood. In this study, a predictive metabolomics framework was applied to investigate the relationship between leaf metabolic profiles and floral traits, focusing on flower colour and floral form. Leaves from 315 individual trees, including 15 Camellia species and representing 1,160 samples, were analysed by untargeted metabolomics, generating a large-scale metabolic profiling dataset. A dedicated quality control strategy was implemented to ensure analytical stability across multiple injection series and flowering seasons. Penalised generalised linear models were used to uncover robust metabolic predictors associated with floral traits and to evaluate model performance through internal and external validation. Distinct sets of metabolites were associated with flower colour and floral form, with limited overlap between traits. Predictive performance was consistently higher for colour than for floral form, indicating more structured metabolic signatures for chromatic traits. The selected predictors spanned multiple major chemical classes, supporting a systemic organisation of the metabolome rather than reliance on single biosynthetic pathways. Consistently high predictive accuracies were obtained, reaching approximately 87% for both flower colour and floral form, and remaining clearly above the corresponding no-information rates ({approx} 43%). Together, these results demonstrate that leaf metabolomics can be used to robustly predict floral traits in Camellia and highlight the potential of predictive metabolomics as a tool for early phenotype inference, quality control and selection in long-lived ornamental species.

plant biology↗

Root phenolics as potential drivers of preformed defenses and reduced disease susceptibility in a paradigm bread wheat mixture

Plant-plant interactions modulate foliar disease susceptibility in intraspecific mixtures. However, the molecular events including signals and responses underlying the reduction in disease susceptibility remain largely unexplored. Here, we developed an experimental system that can abolish root-mediated interactions between plants in a model of bread wheat varietal mixture. We then performed transcriptomic and metabolomic analyses to uncover the molecular responses linked to decreased susceptibility to Septoria tritici blotch in plant-plant interactions. Our analysis revealed that disrupting root chemical interactions impaired the reduction in susceptibility to Septoria and identified phenolic compounds as potential key mediators. The plant-plant interactions under study triggered significant molecular changes in specialized metabolism, biotic interactions, transporters, and responses to resources. Disrupting root interactions canceled both the macroscopic and molecular responses, thus providing a strong link between them. These insights provide a deeper understanding of the molecular basis of plant-plant interactions and the processes involved in reducing disease susceptibility in intraspecific mixtures. Significance statementNeighboring plants mediate resistance to leaf fungal pathogens by releasing root-derived molecules. These interactions trigger multi-omic reprogramming of defenses in both leaves and roots. Enhanced resistance in varietal mixtures is associated with the early activation of defense pathways. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=186 SRC="FIGDIR/small/699261v1_ufig1.gif" ALT="Figure 1"> View larger version (27K): org.highwire.dtl.DTLVardef@16f02a9org.highwire.dtl.DTLVardef@117b872org.highwire.dtl.DTLVardef@4e5243org.highwire.dtl.DTLVardef@1fac682_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical abstractC_FLOATNO C_FIG

plant biology↗

Investigating the intraspecific diversity of Vitis vinifera responses to esca with a physiopathology approach

Woody plant dieback involves complex interactions between pathogens, plant functional traits and environmental conditions. The role of intraspecific variation in functional strategies in shaping susceptibility to dieback remains unclear, despite its importance for understanding plant adaptation to changing environments. We used a common garden containing 46 Vitis vinifera (grapevine) cultivars to test the hypothesis that differences in grapevine susceptibility to esca, a complex vascular disease leading to dieback, result from intraspecific syndromes of leaf gas exchange, wood anatomical and metabolic traits, and microbiome. Cultivars with conservative water use strategies tended to be less susceptible to esca whereas xylem anatomy did not affect esca susceptibility. Across cultivars, symptomatic plants displayed decreases in leaf gas exchange, stem starch storage and theoretical hydraulic conductivity in response to esca. Symptomatic stems accumulated more secondary metabolites (mostly glycosylated flavonoids and terpenes) in highly susceptible than in weakly susceptible genotypes, whereas stem microbial communities were unaffected. This suggests that disease expression is linked to cultivar-specific metabolic responses. Intraspecific variation in physiological strategies contributes to differences in susceptibility to a complex vascular disease. Integrative studies unravelling plant-microorganism-environment interactions are crucial to improve our understanding of complex plant diseases.

plant biology↗

Wood composition, rather than microbial communities, underpins varietal differences in wood degradation and esca foliar symptom expression in grapevine

Deciphering the interplay between microbial communities and host defence mechanisms is key to understanding plant health. In perennial plants, the balance between endophytes and wood (i.e. secondary xylem) defence responses governs wood degradation and vascular disease expression. Esca is a complex vascular disease contributing to grapevine decline, with an incidence variable across cultivars but the mechanisms underlying its expression and varietal susceptibility remain unclear. We assessed relationships between internal wood degradation and esca foliar symptoms in Vitis vinifera L. cultivars grown in a common garden, and, at the cultivar level, we tested for correlations between (i) susceptibility to wood decay and esca expression (n = 16 cultivars) and (ii) wood biochemical traits, and healthy wood endophytic microbial communities (n = 23 cultivars). Unlike other types of necrosis, white-rot necrotic wood was significantly more abundant in plants that had expressed esca leaf symptoms in previous years, particularly in the most susceptible cultivars. These cultivars also contained significantly lower levels of constitutive wood extractives. However, glycosylated phenylpropanoids accumulated in the wood of esca-symptomatic plants, especially in highly susceptible cultivars. By contrast, esca expression and varietal susceptibility had only a marginal effect on the diversity, composition and putative functions of microbial communities in healthy wood. They did not influence either the relative abundance of Fomitiporia mediterranea, the putative causal agent of white-rot in grapevine. Esca susceptibility appears primarily linked to wood degradability and metabolic responses, rather than healthy wood's microbial communities, suggesting that the use of less susceptible varieties together with white-rot removal might attenuate grapevine decline.

plant biology↗

Stress-dependent responses of grapevine wood and fungal pathogen activity under esca and drought

O_LIBiotic and abiotic stresses alter the physiology of perennial plants, with consequences for fungal endophytes and disease expression. In grapevine, one of the worlds most valuable crops, drought inhibits esca disease expression, but the underlying molecular interactions between plant and fungi are unknown. C_LIO_LIWe combined wood metatranscriptomics, metabolomics, and metabarcoding to investigate these interactions in 30-year-old grapevines and eight wood-pathogenic fungi under conditions of drought or esca leaf symptom expression. C_LIO_LIBoth esca and drought decreased grapevine transpiration, but with different transcriptomic and metabolic signatures. Similar pathways were also activated, including the phenylpropanoid and stilbenoid synthesis pathways. These stress responses could potentially confer cross-tolerance, and elicit different fungal molecular responses. The levels of putative fungal virulence factors increased significantly under both stresses. Under drought, only the relative abundance of Phaeomoniella chlamydospora and gene expression involved in anti-oxidative mechanisms, growth, and reproduction increased. Under esca expression conditions, only the relative abundance of Fomitiporia mediterranea and gene expression involved in wood degradation, competition, detoxification, and growth increased. C_LIO_LIThe grapevine defense mechanisms induced by drought coupled with a low transpiration rate and a low abundance and virulence of F. mediterranea may account for esca leaf symptom inhibition upon water deficit. C_LI

plant biology↗

Nitrogen nutrition impacts grapevine esca leaf symptom incidence, physiology and metabolism.

Nitrogen plays a crucial role in plant growth and defence mechanisms, yet its role in plant-pathogen interactions is complex and remains largely unexplored, especially in perennial crops. This study aimed to investigate the effects of controlled nitrogen nutrition levels on disease incidence, fungal communities, and plant physiology and metabolism. Esca is a widespread grapevine vascular disease affecting physiology, xylem integrity and metabolism. Naturally infected Vitis vinifera L. cv. Sauvignon blanc were subjected to three ammonium nitrate treatments across three seasons, resulting in reduced esca incidence under nitrogen deficiency compared with medium nutrition levels, while excess nitrogen had no significant impact. Nitrogen treatments significantly impacted vine physiology and leaf metabolites but did not affect fungal wood communities. Nitrogen deficiency significantly reduced stem diameter, photosynthesis, and leaf area, likely decreasing whole-plant transpiration, while excess nitrogen increased these factors suggesting a key role of plant transpiration in esca incidence. Additionally, nitrogen deficiency led to significantly higher production of phenylpropanoids, particularly flavonoids, in leaf metabolomes compared to the medium level. These findings highlight the pivotal role of nitrogen in the development of esca through alterations in vine morphology, physiology and metabolism. Fertilization practices may be crucial in the management of plant diseases.

plant biology↗

Grapevine cell response to carbon deficiency requires transcriptome and methylome reprogramming

Sugar limitation has dramatic consequences on plant cells, which include a profound reorganization of the cell metabolism, transcriptional reprogramming, and the recycling of cellular components to maintain fundamental cell functions. There is so far no description of the possible contribution of epigenetic regulations in the adaptation of plant cells to limited carbon availability. We investigated this question using non-photosynthetic grapevine cells (Vitis vinifera, cv Cabernet Sauvignon) cultured in vitro with contrasted glucose concentrations. As expected, limited sugar availability in the culture medium led to a rapid cell growth arrest. This was associated with a major metabolic shift characterized by depletion in soluble sugar and total amino acids, an increase in malate content and changes in the cell redox status. Consistently, flux modeling showed a dramatic slowdown of many pathways required for biomass accumulation such as cell wall polymers and total protein content. In contrast, anaplerotic fluxes, the synthesis of some amino acids, redox and polyamine metabolism were enhanced. Carbon deprivation also resulted in a major transcriptional reprogramming characterized by the induction of genes involved in photosynthesis, and the repression of those related to sucrose mobilization or cell cycle control. Similarly, the epigenetic landscape was deeply modified. Glucose-depleted cells showed a higher global DNA methylation level than those grown with glucose. Changes in DNA methylation mainly occurred at transposable elements, but also at genes including differentially expressed genes, suggesting that DNA methylation could participate in the adaptation of cells to limited sugar availability. In addition, genes encoding histone modifiers were differentially expressed suggesting that additional epigenetic mechanisms may be at work during the response of plant cells to carbon shortage.

plant biology↗

Convergent and divergent responses of the rhizosphere chemistry and bacterial communities to a stress gradient in the Atacama Desert.

Plants can modulate their rhizosphere chemistry, thereby influencing microbe communities. Although our understanding of rhizosphere chemistry is growing, knowledge of its responses to abiotic constraints is limited, especially in realistic ecological contexts. Here, we combined predictive metabolomics with bacterial sequencing data to investigate whether rhizosphere chemistry responded to environmental constraints and shaped bacterial communities across an elevation gradient in the Atacama Desert. We found that metabolic adjustments of rhizosphere chemistry predicted the environment of four plant species independently of year, identifying important rhizosphere metabolic biomarkers. Inter-species predictions unveiled significant biochemical convergences. Subsequently, we linked metabolic predictors to variation in the abundance of operational taxonomic units (OTUs). Chemical response influenced distinct and common bacterial families between species and vegetation belts. The annotation of chemical markers and correlated bacterial families highlighted critical biological processes such as nitrogen starvation, metal pollution and plant development and defence. Overall, this study demonstrates a unique metabolic set likely involved in improving plant resilience to harsh edaphic conditions. Besides, the results emphasise the need to integrate ecology with plant metabolome and microbiome approaches to explore plant-soil interactions and better predict their responses to climate change and consequences for ecosystem dynamics.

ecology↗

Phylogenetically diverse wild plant species use common biochemical strategies to thrive in the Atacama Desert

The best ideotypes are under mounting pressure due to increased aridity in many parts of the world. Understanding the conserved molecular mechanisms that evolve in wild plant species adapted to harsh environments is crucial in developing new strategies for sustainable agriculture. Yet our knowledge of such mechanisms in wild species is scant, particularly in extreme environments. We performed metabolic pathway reconstruction using transcriptome information from 32 Atacama plant species and phylogenetically related plant species that do not live in Atacama (Sister species). We analyzed pathway and reaction enrichment to understand the biochemical commonalities and differences of wild Atacama plant species. To gain insights into the mechanisms that ensure plant survival, we compared expressed gene isoform numbers and gene expression patterns between the annotated biochemical reactions from 32 Atacama and Sister species. We found significant biochemical convergences in primary and secondary metabolism characterized by reactions enriched in at least 50% of the Atacama species across major plant phylogenetic lineages. Analysis of the annotation indicated potential advantages against drought, salinity, high solar irradiance, and nitrogen starvation. These findings suggest that the adaptation in the Atacama Desert may result in part from shared genetic legacies governing the expression of key metabolic pathways to face harsh environmental conditions. Enriched reactions corresponded to ubiquitous compounds common to extreme and agronomic species and were congruent with our previous metabolomic analyses in these Atacama species. Hence, genes underlying these adaptive traits offer promising candidates for improving abiotic stress resilience in crop species.

plant biology↗

Blue light promotes ascorbate synthesis by deactivating the PAS/LOV photoreceptor that inhibits GDP-L-galactose phosphorylase

Ascorbate (vitamin C) is one of the most essential antioxidants in fresh fruits and vegetables. To get insights into the regulation of ascorbate metabolism in plants, a mutant producing ascorbate-enriched fruits was studied. The causal mutation, identified by a mapping-by-sequencing strategy, corresponded to a knock-out recessive mutation in a new class of photoreceptor named PAS/LOV protein (PLP, Solyc05g07020), which acts as a negative regulator of ascorbate biosynthesis in tomato. This trait was confirmed by CRISPR/Cas9 gene editing, and further found in all plant organs, including fruit that accumulated 2-3 times more ascorbate than in the WT. The functional characterization revealed that PLP interacted with the two isoforms of GDP-L-galactose phosphorylase (GGP), known as the controlling step of the L-galactose pathway of ascorbate synthesis. The interaction with GGP occurred in the cytoplasm and the nucleus, but was abolished when PLP was mutated. These results were confirmed by an optogenetic approach using an animal cell system, which additionally demonstrated that blue light modulated the PLP-GGP interaction. Assays performed in vitro with heterologously expressed GGP and PLP showed that PLP is a non-competitive inhibitor of GGP that is inactivated after blue light exposure. This discovery sheds light on the light-dependent regulation of ascorbate metabolism in plants.

plant biology↗