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Glauser, G.

Publications and source records attributed to Glauser, G..

At least 19 recordsLinked to original sources

Rapid green leaf volatile sensing allows intact plants to release induced volatiles earlier than wounded emitters

Organisms in the vicinity of attacked neighbors can respond to danger cues by activating their own defenses. However, the temporal dynamics of these interactions remain poorly resolved, despite their importance for the ensuing effects. Here, we investigated defense responses of maize plants that are exposed to induced volatiles from herbivory-induced neighbors in real time. These experiments revealed a surprising temporal paradox: Intact neighbors start emitting most induced volatiles 15-80 min earlier than the attacked plants themselves. This earlier responsiveness was not associated with earlier induction of defense hormones, volatile biosynthesis genes or within-leaf volatile accumulation. Instead, receiver plants kept their stomata open, while attacked sender plants rapidly closed them to combat water loss. Using different volatile deficient mutants, we demonstrate that the rapid responses in receivers are triggered by green leaf volatiles, which are released from the wound sites of sender plants within minutes independently of stomatal aperture. Thus, non-attacked neighbors can act as "unhindered observers" that activate some defenses more quickly than attacked organisms themselves, as they do not have to deal with wound trauma. The resulting plant volatile concatenation patterns expand our understanding of volatile signaling and have the potential to shape population-level multitrophic interactions.

plant biology↗

Photorhabdus metabolites reshape soil microbial communities and promote plant growth and insect resistance

Photorhabdus bacteria are potent insect-killing microbes associated with entomopathogenic nematodes and offer opportunities for environmentally benign pest control. They can be applied as foliar sprays or soil drenches without their nematode vector, resulting in massive amounts of Photorhabdus cells and their (toxic) metabolites introduced into the soil. However, their effects beyond the target organisms are unknown. To fill this knowledge gap, we investigated the soil legacy effects of Photorhabdus cells and their metabolites on soil microbial communities, plant performance and resistance to herbivores. To this end, we first conditioned soils with i) mechanically killed (MK) or Photorhabdus-infected insect larvae, ii) aqueous extracts of MK or Photorhabdus-infected insect larvae, iii) cell-free Photorhabdus supernatants, iv) autoclaved soil complemented with live soil previously conditioned with MK or Photorhabdus-infected insect larvae. We then grew maize plants in these soils and measured plant biomass, profiled soil microbial communities and plant metabolites, and evaluated plant resistance against two pest insects Diabrotica balteata and Spodoptera frugiperda. We found that conditioned soils increased plant biomass by 10-26% relative to controls and significantly altered soil bacterial and nematode communities, and to a lesser extent, fungal communities. Re-inoculating conditioned soil microbiota into autoclaved soils recreated the plant growth-promoting effects, indicating microbial-mediated mechanisms. Additionally, plants grown in soils conditioned with Photorhabdus-infected insect cadavers were often more resistant to herbivorous insect attack, in a strain-specific manner. On average, D. balteata and S. frugiperda larvae gained 10-20% and 10-59% less weight, respectively, when fed on plants grown in conditioned soils than on plants grown in control soils. The plant metabolic profiles of plant leaves and roots also varied with resistance levels. We conclude that Photorhabdus metabolites modulate soil microbial communities towards a structure that enhances plant growth and triggers systemic responses against herbivores.

microbiology↗

Conservation and divergence of UVR8-COP1/SPA-HY5 signaling in UV-B responses of Marchantia polymorpha

Ultraviolet-B radiation (UV-B) poses a major challenge to all forms of plant life. The liverwort Marchantia polymorpha (Marchantia) serves as a key model organism to study signaling pathways and to infer their evolution throughout the green lineage. Marchantia expresses key components of UV-B signaling, including the photoreceptor UV RESISTANCE LOCUS 8 (MpUVR8), the WD40-repeat protein REPRESSOR OF UV-B PHOTOMORPHOGENESIS (MpRUP), the E3 ubiquitin ligase complex CONSTITUTIVELY PHOTOMORPHOGENIC 1 / SUPPRESSOR OF phyA-105 (MpCOP1/MpSPA), and the transcriptional regulator ELONGATED HYPOCOTYL 5 (MpHY5). Here, we show that MpUVR8 exists as a homodimer in its ground-state in vivo, then monomerizes and accumulates in the nucleus upon UV-B activation. Activated MpUVR8 interacts with MpCOP1, triggering growth inhibition, genome-wide gene expression changes, biosynthesis of UV-absorbing metabolites, and photoprotection, which overall contributes to UV-B stress tolerance. MpRUP facilitates redimerization of MpUVR8 and Mprup null mutants show enhanced UV-B photomorphogenesis, demonstrating that MpRUP efficiently represses MpUVR8 signaling. Unlike the case in Arabidopsis and in contrast to the strong Mpcop1 mutant phenotype, Mpspa mutants develop only a very weak constitutive photomorphogenesis phenotype, indicating that COP1 function is much more independent of SPA in Marchantia than in Arabidopsis. Moreover, in contrast to Arabidopsis SPAs, Mpspa is linked with a hyper-responsive UV-B phenotype, suggesting that MpSPA is a negative regulator of MpUVR8 signaling. Similar to Arabidopsis HY5/HYH, MpHY5 functions antagonistically to MpCOP1, but its role in UV-B-mediated gene expression changes is more limited. Our findings demonstrate that although core components of UV-B signaling existed in the last common ancestor of extant land plants, regulatory interactions have diversified in different lineages since their divergence more than 400 million years ago.

plant biology↗

Wheat infection by Fusarium graminearum species complex members is facilitated by a transcriptionally conserved non-ribosomal peptide synthetase gene cluster

Biosynthetic gene clusters (BGCs) are often found in fungal pathogens and encode secondary (or specialized) metabolites that play crucial roles in host and niche adaptation. However, the regulatory dynamics and functions of these BGCs during host infection remain largely unknown. To address this gap, we employed interspecies comparative transcriptomics to identify BGCs involved in host-pathogen interactions mediated by the Fusarium graminearum species complex (FGSC). We conducted joint transcriptomic and metabolomic analyses during wheat infection and in vitro experiments with five members of the FGSC to understand gene regulation during host infection. Our findings revealed that expression regulation was predominantly species-specific, but we also identified a set of shared upregulated genes that were common to all five FGSC species showing enrichment for metabolic and pathogenicity-associated functions. We focused on jointly upregulated BGC during infection and identified a NRPS-like gene cluster named SM3. The cluster was highly conserved within FGSC and shared by the more distant F. sambucinum species complex. We show that inactivation of the BGC core gene significantly impairs F. graminearum sensu stricto (s.s.) spore production, reduces fungal spread and Fusarium Head Blight symptoms on wheat kernels. Our results highlight that comparative infection transcriptomes can reveal conserved metabolic functions mediating the host infection process of a plant pathogen.

microbiology↗

plantMASST - Community-driven chemotaxonomic digitization of plants

Understanding the distribution of hundreds of thousands of plant metabolites across the plant kingdom presents a challenge. To address this, we curated publicly available LC-MS/MS data from 19,075 plant extracts and developed the plantMASST reference database encompassing 246 botanical families, 1,469 genera, and 2,793 species. This taxonomically focused database facilitates the exploration of plant-derived molecules using tandem mass spectrometry (MS/MS) spectra. This tool will aid in drug discovery, biosynthesis, (chemo)taxonomy, and the evolutionary ecology of herbivore interactions.

plant biology↗

Natural soil suppressiveness against soilborne phytopathogens extends to the control of insect pest

Since the 1980s, soils in a 22-km2 area near Lake Neuchatel in Switzerland have been recognized for their innate ability to suppress the black root rot plant disease. Their efficacy against insect pests has not been studied. We demonstrate that natural soil suppressiveness also protects plants from the leaf-feeding pest insect Oulema melanopus. Plants grown in the most suppressive soil have a reduced stress response to Oulema feeding, reflected by dampened levels of herbivore defense-related phytohormones and benzoxazinoids, and enhanced salicylate levels in plants without the insect indicate defense-priming. The rhizosphere microbiome network of the suppressive soils was highly tolerant to the destabilizing impact of insect exposure. The presence of plant-beneficial bacteria in the suppressive soils along with priming conferred plant resistance to the insect pest, manifesting also in the onset of insect microbiome dysbiosis. This intricate soil-plant-insect feedback extends natural soil suppressiveness from soilborne diseases to insect pests.

plant biology↗

Photoreceptor-induced sinapate synthesis contributes to photoprotection in Arabidopsis

Plants must balance light capture for photosynthesis with protection from potentially harmful ultraviolet radiation (UV). Photoprotection is mediated by concerted action of photoreceptors, but the underlying molecular mechanisms are not fully understood. In this study, we provide evidence that UV RESISTANCE LOCUS 8 (UVR8) UV-B-, phytochrome red-, and cryptochrome blue-light photoreceptors converge on the induction of FERULIC ACID 5-HYDROXYLASE 1 (FAH1) that encodes a key enzyme in the phenylpropanoid biosynthesis pathway, leading to the accumulation of UV-absorbing sinapate esters. FAH1 induction depends on the bZIP transcription factors ELONGATED HYPOCOTYL 5 (HY5) and HY5-HOMOLOG (HYH) that function downstream of all three photoreceptors. Noticeably, mutants with hyperactive UVR8 signalling rescue fah1 UV sensitivity. Targeted metabolite profiling suggests that this phenotypic rescue is due to the accumulation of UV-absorbing metabolites derived from precursors of sinapate synthesis, namely coumaroyl-glucose and feruloyl-glucose. Our genetic dissection of the phenylpropanoid pathway combined with metabolomic and physiological analyses show that both sinapate esters and flavonoids contribute to photoprotection with sinapates playing a major role for UV screening. Our findings indicate that photoreceptor-mediated regulation of FAH1 and subsequent accumulation of sinapate "sunscreen" compounds is a key protective mechanism to mitigate damage, preserving photosynthetic performance, and ensuring plant survival under UV.

plant biology↗

The benzoxazinoid breakdown product 5-Methoxy-2-Nitrophenol has a dual function in maize defense against herbivory

Catabolism of plant secondary metabolites can yield bioactive breakdown products. However, these compounds often remain poorly characterized. Here, we report on the discovery, biosynthesis, and biological relevance of 5-Methoxy-2-Nitrophenol (5M2NP), a secondary metabolite breakdown product which accumulates in damaged maize tissues. We used mutant plants, biochemical complementation, and metabolomic analyses to determine the biosynthetic origin of 5M2NP. Additionally, we assessed 5M2NPs role in plant defense against herbivores. For this, we surveyed defense-associated responses (gene expression, phytohormones, volatile organic compounds) in wounded, 5M2NP-supplemented maize leaves, and performed bioassays with herbivorous insects. We found that 5M2NP accumulation upon tissue disruption is contingent upon a functional benzoxazinoid biosynthesis pathway. Labeling experiments demonstrated that 5M2NP is derived from DIMBOA. Physiological doses of exogenous 5M2NP increased the wound-induced expression of defense genes and emission of terpenoids. Additionally, 5M2NP exhibited antibiotic and antixenotic activities towards both generalist and specialist herbivores in nano-to micromolar quantities. We conclude that 5M2NP, which represents a novel class of plant-derived compounds, can act as a direct defense and a defense modulator. 5M2NP thus expands the functional repertoire of benzoxazinoids and likely contributes to their protective function against insect herbivores. The discovery of 5M2NP highlights the multifunctionality of plant secondary metabolites and their breakdown products.

plant biology↗

Leaf metabolic traits reveal hidden dimensions of plant form and function

The plant metabolome encompasses the biochemical mechanisms through which evolutionary and ecological processes shape plant form and function1,2. However, while the metabolome should thus be an important component of plant life-history variation3, we know little about how it varies across the plant kingdom. Here, we use the plant functional trait concept4 - a powerful framework for describing plant form and function5-7 - to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five discriminant metabolic functional traits reveals that plants vary along two major axes of leaf metabolic specialization - a leaf chemical defense spectrum and an expression of leaf longevity. These axes are qualitatively consistent for tropical and temperate species, with many trait combinations being viable. However, axes of leaf metabolic specialization vary orthogonally to life-history strategies described by widely used functional traits5-7, while being at least equally important to them. Our findings question classical trait6 and plant defense8 theory that predicts relationships between the leaf chemical phenotype, plant productivity, and pace of life. Moreover, we show that metabolic functional traits describe unique dimensions of plant life-history variation that are complementary to, and independent from, those captured by existing plant functional traits.

ecology↗

Plant secondary metabolite-dependent plant-soil feedbacks can improve crop yield in the field

Plant secondary metabolites that are released into the rhizosphere alter biotic and abiotic soil properties, which in turn affect the performance of other plants. How such plant-soil feedbacks affect agricultural productivity and food quality in crop rotations is unknown. Here, we assessed the impact of maize benzoxazinoids on the performance, yield and food quality of three winter wheat varieties in a two-year field experiment. Following maize cultivation, we detected benzoxazinoid-dependent chemical and microbial fingerprints in the soil. The chemical fingerprint was still visible during wheat growth, while the microbial fingerprint was no longer detected. Benzoxazinoid soil conditioning by wild-type maize led to increased wheat emergence, tillering, growth and biomass compared to soil conditioning by bx1 mutant plants. Weed cover remained unaffected, while insect damage decreased in a subset of varieties. Wheat yield was increased by over 4% without a reduction in grain quality across varieties. This improvement was directly associated with increased germination and tillering. Taken together, our experiments demonstrate that plant secondary metabolites can increase yield via plant-soil feedbacks under agronomically realistic conditions. If this phenomenon holds across different soils and environmental conditions, optimizing plant root exudation could be a powerful, genetically tractable strategy to enhance crop yields without additional inputs.

plant biology↗

Chromoplast plastoglobules recruit the carotenoid biosynthetic pathway and contribute to carotenoid accumulation during tomato fruit maturation

Tomato (Solanum lycopersicum) fruit maturation is associated with a developmental transition from chloroplasts (in mature green fruit) to chromoplasts (in red fruit). The hallmark red color of ripe tomatoes is due to carotenogenesis and accumulation of the red carotenoid lycopene inside chromoplasts. Plastoglobules (PG) are lipid droplets in plastids that are involved in diverse lipid metabolic pathways. In tomato, information on the possible role of PG in carotogenesis and the PG proteome is largely lacking. Here, we outline the role of PG in carotenogenesis giving particular attention to tomato fruit PG proteomes and metabolomes. The proteome analysis revealed the presence of PG-typical FBNs, ABC1K-like kinases, and metabolic enzymes, and those were decreased in the PG of tomato chromoplasts compared to chloroplasts. Notably, the complete {beta}-carotene biosynthesis pathway was recruited to chromoplast PG, and the enzymes PHYTOENE SYNTHASE 1 (PSY-1), PHYTOENE DESATURASE (PDS), ZETA-CAROTENE DESATURASE (ZDS), and CAROTENOID ISOMERASE (CRTISO) were enriched up to twelvefold compared to chloroplast PG. We profiled the carotenoid and prenyl lipid changes in PG during the chloroplast to chromoplast transition and demonstrated large increases of lycopene and {beta}-carotene in chromoplast PG. The PG proteome and metabolome are subject to extensive remodeling resulting in high accumulation of lycopene during the chloroplast-to-chromoplast transition. Overall, the results indicate that PGs contribute to carotenoid accumulation during tomato fruit maturation and suggest that they do so by functioning as a biosynthetic platform for carotenogenesis.

plant biology↗

Maize integrates light and volatile cues from neighboring plants into unique defense responses

Plants perceive the presence and defense status of their neighbors through light and volatile cues, but how plants integrate both stimuli is poorly understood. We investigated if and how low Red to Far red light (R:FR) ratios, indicative of shading or canopy closure, affect maize (Zea mays) responses to herbivore-induced plant volatiles (HIPVs), including the green leaf volatile (Z)-3-hexenyl acetate. We modulated light signaling and perception by using FR supplementation and a phyB1phyB2 mutant, and we determined volatile release as a response readout. To gain mechanistic insights, we examined expression of volatile biosynthesis genes, hormone accumulation, and photosynthesis. Exposure to a full blend of HIPVs or (Z)-3-hexenyl acetate induced maize volatile release. Short-term FR supplementation increased this response. In contrast, prolonged FR supplementation or constitutive phytochrome B inactivation in phyB1phyB2 plants showed the opposite response. Short-term FR supplementation enhanced photosynthesis and stomatal conductance and (Z)-3-hexenyl acetate-induced JA-Ile levels. We conclude that a FR-enriched light environment can prompt maize plants to respond more strongly to HIPVs emitted by neighbors, which might be explained by changes in photosynthetic processes and phytochrome B signaling. Our findings reveal interactive responses to light and volatile cues with potentially important consequences for plant-plant and plant-herbivore interactions.

plant biology↗

Novel insights on the contribution of plastoglobules and reactive oxygen species to chromoplast differentiation

Enriching plant tissues in phytonutrients can be done by stimulating their biosynthesis but also by providing appropriate sink structures for their sequestering and storage. Chromoplasts are plastids specialized in the production and accumulation of carotenoids that are naturally formed in non-photosynthetic tissues such as flower petals and ripe fruit. Chromoplasts can also be artificially differentiated from leaf chloroplasts by boosting the production of phytoene (the first committed intermediate of the carotenoid pathway) with the bacterial phytoene synthase crtB. Here we show that crtB-induced leaf chromoplasts develop plastoglobules harboring high levels of carotenoids (mainly phytoene and pro-vitamin A {beta}-carotene) but also other nutritionally-relevant isoprenoids such as tocopherols (vitamin E) and phylloquinone (vitamin K1). Further promoting plastoglobule proliferation by exposure to intense (high) light resulted in a higher accumulation of these health-related metabolites but also an acceleration of the chloroplast-to-chromoplast conversion. We further show that production of reactive oxygen species (ROS) stimulates chromoplastogenesis. Our data suggest that, similar to that already described for decreased photosynthesis and enhanced carotenoid biosynthesis, ROS production is not just a consequence but a promoter of the chromoplast differentiation process.

plant biology↗

The Arabidopsis endosperm is a temperature-sensing tissue that implements seed thermoinhibition through phyB and PIF3

Seed thermoinhibition, the repression of germination under high temperatures, prevents seedling establishment under potentially fatal conditions. Thermoinhibition is relevant for ecology, phenology and agriculture, particularly in a warming globe. The temperature sensing mechanisms and signaling pathways sustaining thermoinhibition are unknown. We found that thermoinhibition in Arabidopsis thaliana is not autonomously controlled by the embryo but is rather implemented by the endosperm surrounding the embryo. High temperature is sensed through endospermic phyB by accelerating its reversion from the active signaling Pfr form into the inactive Pr form, as described in seedlings. This leads to stabilization of endospermic PIF3, which represses the expression of the endospermic ABA catabolic gene CYP707A1 and promotes endospermic ABA synthesis and release towards the embryo to block its growth. Furthermore, endospermic ABA represses embryonic PIF3 accumulation that would otherwise promote embryonic growth. Hence, under high temperatures PIF3 exerts opposite growth responses in the endosperm and embryo.

plant biology↗

Genome-wide association mapping reveals genes underlying population-level metabolome diversity in a fungal crop pathogen

BackgroundFungi produce a wide range of specialized metabolites (SMs) involved in biotic interactions. Pathways for the production of SMs are often encoded in clusters of tightly arranged genes identified as biosynthetic gene clusters. Such gene clusters can undergo horizontal gene transfers between species and rapid evolutionary change within species. The acquisition, rearrangement and deletion of gene clusters can generate significant metabolome diversity. However, the genetic basis underlying variation in SM production remains poorly understood. ResultsHere, we analyzed metabolite production of a large population of the fungal pathogen of wheat, Zymoseptoria tritici. The pathogen causes major yield losses and shows variation in gene clusters. We performed untargeted ultra-high performance liquid chromatography-high resolution mass spectrometry to profile the metabolite diversity among 102 isolates of the same species. We found substantial variation in the abundance of the detected metabolites among isolates. Integrating whole-genome sequencing data, we performed metabolite genome-wide association mapping to identify loci underlying variation in metabolite production (i.e. metabolite-GWAS). We found that significantly associated SNP reside mostly in coding and gene regulatory regions. Associated genes encode mainly transport and catalytic activities. The metabolite-GWAS identified also a polymorphism in the 3UTR region of a virulence gene related to metabolite production and showing expression variation. ConclusionsTaken together, our study provides a significant resource to unravel polymorphism underlying metabolome diversity within a species. Integrating metabolome screens should be feasible for a range of different plant pathogens and help prioritize molecular studies.

microbiology↗

Photosynthetic light harvesting and thylakoid organization in a CRISPR/Cas9 Arabidopsis thaliana LHCB1 knockout mutant.

Light absorbed by chlorophylls of photosystem II and I drives oxygenic photosynthesis. Light-harvesting complexes increase the absorption cross-section of these photosystems. Furthermore, these complexes play a central role in photoprotection by dissipating the excess of absorbed light energy in an inducible and regulated fashion. In higher plants, the main light-harvesting complex is the trimeric LHCII. In this work, we used CRISPR/Cas9 to knockout the five genes encoding LHCB1, which is the major component of the trimeric LHCII. In absence of LHCB1 the accumulation of the other LHCII isoforms was only slightly increased, thereby resulting in chlorophyll loss leading to a pale green phenotype and growth delay. Photosystem II absorption cross-section was smaller while photosystem I absorption cross-section was unaffected. This altered the chlorophyll repartition between the two photosystems, favoring photosystem I excitation. The equilibrium of the photosynthetic electron transport was partially maintained by a lower photosystem I over photosystem II reaction center ratio and by the dephosphorylation of LHCII and photosystem II. Loss of LHCB1 altered the thylakoid structure, with less membrane layers per grana stack and reduced grana width. Stable LHCB1 knock out lines allow characterizing the role of this protein in light harvesting and acclimation and pave the way for future in vivo mutational analyses of LHCII.

plant biology↗

Soil composition and plant genotype determine benzoxazinoid-mediated plant-soil feedbacks in cereals

Plant-soil feedbacks refer to effects on plants that are mediated by soil modifications caused by the previous plant generation. Maize conditions the surrounding soil by secretion of root exudates including benzoxazinoids (BXs), a class of bioactive secondary metabolites. Previous work found that a BX- conditioned soil microbiota enhances insect resistance while reducing biomass in the next generation of maize plants. Whether these BX-mediated and microbially driven feedbacks are conserved across different soils and response species is unknown. We found the BX-feedbacks on maize growth and insect resistance conserved between two arable soils, but absent in a more fertile grassland soil, suggesting a soil-type dependence of BX feedbacks. We demonstrated that wheat also responded to BX-feedbacks. While the negative growth response to BX-conditioning was conserved in both cereals, insect resistance showed opposite patterns, with an increase in maize and a decrease in wheat. Wheat pathogen resistance was not affected. Finally and consistent with maize, we found the BX-feedbacks to be cultivar specific. Taken together, BX- feedbacks affected cereal growth and resistance in a soil and genotype dependent manner. Cultivar-specificity of BX-feedbacks is a key finding, as it hides the potential to optimize crops that avoid negative plant-soil feedbacks in rotations.

plant biology↗

A triresidue motif in the GLUTAMATE RECEPTOR-LIKE 3.3 C-tail interacts with IMPAIRED SUCROSE INDUCTION 1 and controls long distance wound signaling

Arabidopsis Clade 3 GLUTAMATE RECEPTOR-LIKE (GLRs) genes are primary players in wound-induced electrical signaling and jasmonate-activated defense responses. As cation-permeable ion channels, previous studies have focused on resolving their gating properties and structures. However, little is known regarding to the regulatory mechanism of these channel proteins. Here, we report that the C-tail of GLR3.3 contains key elements that control its function in long distance wound signaling. GLR3.3 without its C-tail failed to rescue the glr3.3a mutant. To further investigate the underlying mechanism, we performed a yeast two-hybrid screen. IMPAIRED SUCROSE INDUCTION 1 (ISI1) was identified as an interactor with both the C-tail and the full-length GLR3.3 in planta. Reduced function isi1 mutants had enhanced electrical activity and jasmonate-regulated defense responses. Furthermore, we found that a triresidue motif RFL (R884, F885 and L886) in the GLR3.3 C-tail is essential for interacting with ISI1. RFL mutation abolished GLR3.3 function in electrical signaling and jasmonate-mediated defense gene activation. Our study shows the importance of the C-tail in GLR3.3 function, and reveals parallels with the ipnotropic glutamate receptor regulation in animal cells.

plant biology↗