Biology subjects

Robert, C. A. M.

Publications and source records attributed to Robert, C. A. M..

7 recordsLinked to original sources

bioRxiv2023

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↗

bioRxiv2023

Bacterial tolerance to host-exuded specialized metabolites structures the maize root microbiome

Plants exude specialized metabolites from their roots and these compounds are known to structure the root microbiome. However, the underlying mechanisms are poorly understood. We established a representative collection of maize root bacteria and tested their tolerance against benzoxazinoids, the dominant specialized and bioactive metabolites in the root exudates of maize plants. In vitro experiments revealed that benzoxazinoids inhibited bacterial growth in a strain- and compound-dependent manner. Tolerance against these selective antimicrobial compounds depended on bacterial cell wall structure. Further, we found that native root bacteria isolated from maize tolerated the benzoxazinoids better compared to non-host Arabidopsis bacteria. This finding suggests the adaptation of the root bacteria to the specialized metabolites of their host plant. Bacterial tolerance to 6-methoxy-benzoxazolin-2-one (MBOA), the most abundant and selective antimicrobial metabolite in the maize rhizosphere, correlated significantly with the abundance of these bacteria on benzoxazinoid-exuding maize roots. Thus, strain-dependent tolerance to benzoxazinoids largely explained the abundance pattern of bacteria on maize roots. Abundant bacteria generally tolerated MBOA, while low abundant root microbiome members were sensitive to this compound. Our findings reveal that tolerance to plant specialized metabolites is an important competence determinant for root colonization. We propose that bacterial tolerance to plant-secreted antimicrobial compounds is an underlying mechanism determining the structure of host-specific microbial communities. Significance StatementDiverse microbial communities colonize plant roots. They feed on carbon rich root exudates which contain a diverse mix of chemicals including primary and specialized metabolites. Here we show that specialized metabolites act as selective antibiotics to shape the root bacterial communities. By growing single isolates of maize root bacteria in the presence of benzoxazinoids in vitro, we find that the strains differ greatly in their tolerance to benzoxazinoids. Their different levels of tolerance largely explained their abundance on benzoxazinoid-exuding roots. Our work shows how plant specialized metabolites act to shape the maize root microbial community and thus deepened our mechanistic understanding of how plants shape their microbiome.

microbiology↗

bioRxiv2022

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↗

bioRxiv2022

A reductase in the lipid metabolism at cross roads between cuticular wax production and jasmonic acid-mediated defenses in maize

Cuticular wax is the first physical layer to protect plants from herbivore infestations. Although wax and jasmonic acid (JA) biosynthesis are the two most studied branches of lipid metabolism, the mechanism how cuticular wax production modulates plant chemical defenses is unclear. Here, we show that the maize (Zea mays) GL8 gene, encoding 3-ketoacyl reductase during fatty acid elongation in the biosynthesis of very long chain fatty acids (VLCFA), functions as a turning point between wax production and JA-mediated defenses. The fall armyworm (Spodoptera frugiperda) larvae consumed more tissue but gained a lower performance on gl8/Ye478 mutant plants. gl8/Ye478 mutant displayed higher JA-mediated defenses constitutively, and also more inducible by herbivore stimulation. The comprehensive transcriptomic and lipidomic analyses further demonstrated that ZmGL8 mutation up-regulates the JA biosynthesis pathway by promoting the accumulation of lysophospholipids and modulation of galactolipid synthase genes ZmDGD and ZmMGD. The phenotypic and transcription comparisons of the maize and Arabidopsis wax-deficient mutants suggest a conserved wide-spread trade-off between wax production and chemical defense in both 18:3 and 16:3 plants. These results illustrate a critical role of VLCFA metabolism as a switch to control the balance between cuticular wax physical barrier and JA-mediated chemical defenses during plant-herbivore coevolution history.

plant biology↗

bioRxiv2020

Integration of plant primary and secondary metabolites as fitness-relevant foraging cues for a specialist herbivore

Plants produce complex mixtures of primary and secondary metabolites. Herbivores use these metabolites as behavioral cues to increase their fitness. However, how herbivores integrate different metabolite classes into fitness-relevant foraging decisions in planta is poorly understood. We developed a molecular manipulative approach to modulate the availability of sugars and benzoxazinoid secondary metabolites as foraging cues for a specialist maize herbivore, the western corn rootworm. By disrupting sugar perception in the western corn rootworm and benzoxazinoid production in maize, we show that sugars and benzoxazinoids act as distinct and dynamically integrated mediators of short-distance host finding and acceptance. While sugars improve the capacity of rootworm larvae to find a host plant and to distinguish post-embryonic from less nutritious embryonic roots, benzoxazinoids are specifically required for the latter. Host acceptance in the form of root damage is increased by benzoxazinoids and sugars in an additive manner. This pattern is driven by increasing damage to post-embryonic roots in the presence of benzoxazinoids and sugars. Benzoxazinoid- and sugar-mediated foraging directly improves western corn rootworm growth and survival. Interestingly, western corn rootworm larvae retain a substantial fraction of their capacity to feed and survive on maize plants even when both classes of chemical cues are almost completely absent. This study unravels fine-grained differentiation and integration of primary and secondary metabolites into herbivore foraging and documents how the capacity to compensate for the lack of important chemical cues enables a specialist herbivore to survive within unpredictable metabolic landscapes.

animal behavior and cognition↗

bioRxiv2019

Plant defense resistance in natural enemies of a specialist insect herbivore

Plants defend themselves against herbivores through the production of toxic and deterrent metabolites. Adapted herbivores can tolerate and sequester these metabolites, allowing them to feed on defended plants and become toxic to their own enemies. Can herbivore natural enemies overcome sequestered plant defense metabolites to prey on adapted herbivores? To address this question, we studied how entomopathogenic nematodes cope with benzoxazinoid defense metabolites that are produced by grasses and sequestered by a specialist maize herbivore, the western corn rootworm. We find that nematodes from US maize fields in regions in which the western corn rootworm was present over the last 50 years are behaviorally and metabolically resistant to sequestered benzoxazinoids and more infective towards the western corn rootworm than nematodes from other parts of the world. Exposure of a benzoxazinoid-susceptible nematode strain to the western corn rootworm for five generations results in higher behavioral and metabolic resistance and benzoxazinoid-dependent infectivity towards the western corn rootworm. Thus, herbivores that are exposed to a plant defense sequestering herbivore can evolve both behavioral and metabolic resistance to plant defense metabolites, and these traits are associated with higher infectivity towards a defense sequestering herbivore. We conclude that plant defense metabolites that are transferred through adapted herbivores may result in the evolution of resistance in herbivore natural enemies. Our study also identifies plant defense resistance as a novel target for the improvement of biological control agents.

plant biology↗

bioRxiv2019

Adapted dandelions increase seed dispersal when they are attacked by root herbivores

Plants allow their offspring to escape unfavourable local conditions through seed dispersal. Whether plants use this strategy to escape herbivores is not well understood. Here, we explore how different Taraxacum officinale populations modify seed dispersal in response to root herbivore attack by Melolontha melolontha in the field. Root herbivore attack increases seed dispersal potential through a reduction in seed weight in populations that have evolved under high root herbivore pressure, but not in populations that have evolved under low pressure. This increase in dispersal potential is associated with reduced germination, suggesting that adapted plants trade dispersal for establishment. Analysis of vegetative growth parameters suggests that increased dispersal is not the result of stress flowering. These results suggest that root herbivory selects for genotypes that increase their dispersal ability in response to herbivore attack.

ecology↗