Biology subjects

Schimmel, B. C. J.

Publications and source records attributed to Schimmel, B. C. J..

6 recordsLinked to original sources

bioRxiv2024

Volatiles from low R:FR-treated maize plants increase the emission of herbivore-induced plant volatiles in their neighbors

Low Red (R) to Far Red (FR) light ratios, a light signal associated with vegetation shade, can prompt intact maize (Zea mays) plants to constitutively emit more volatiles when exposed to herbivory-induced plant volatiles (HIPVs). Here we investigated how simulated shading affects priming responses in the context of volatile-mediated plant-plant interactions. Receiver maize plants were exposed to either constitutive volatile organic compounds (cVOCs) or HIPVs from emitter maize plants, while we manipulated R:FR light conditions of receivers or emitters. Priming responses in the receivers were then assessed by measuring real-time volatile emissions following simulated herbivory. We show that low R:FR light enhances HIPVs emissions in plants previously exposed to HIPVs from neighbours independently of the light conditions of emitters. We also demonstrate that both cVOCs and HIPVs emitted by maize grown under low R:FR amplify HIPVs emissions in their neighbours. This amplified response could not be explained by FR-mediated changes in the release of green leaf volatiles or terpenoids by emitters, thus suggesting the involvement of other VOCs. We conclude that volatile-mediated plant-plant interactions can be expected to become more intense in denser canopies due to light-mediated amplification of volatile emission and responsiveness.

plant biology↗

bioRxiv2024

Competitor Displacement by an Herbivore that Manipulates Plant Defences

Tetranychus evansi is an herbivorous mite specialised on solanaceous hosts, although it has also been observed to colonise non-solanaceous species. It has the ability to suppress the defences of tomato (Solanum lycopersicum), and it can displace competitors from this host using a diverse array of traits. T. evansi is an invasive species in Africa and Europe, where it often displaces native species. While recent evidence suggests that T. evansi can also suppress defences of non-solanaceous hosts, there is a lack of understanding of the molecular changes induced upon mite infestation on hosts other than tomato, as well as how these changes may impact populations of competing herbivores. Here, we investigate the transcriptomic and metabolomic responses of bean (Phaseolus vulgaris) to T. evansi infestation and to T. urticae infestation, a cosmopolitan congeneric that often competes with T. evansi for hosts in areas of co-occurrence. We ask whether the presence of T. evansi facilitates bean colonization for T. urticae, and whether the spatial distribution of mite feeding sites depends on the presence of competitors on bean leaves. We examine whether this facilitation is attributed to jasmonic acid (JA) or salicylic acid (SA) defences by treating plants with exogenous SA and JA and comparing the transcriptomes and metabolomes of bean exposed to either phytohormones or to mite feeding. Finally, we measure phytohormone concentrations and the expression of JA- and SA-responsive genes in plants infested with either mite species or co-infested with both, at different spatial scales. We found that, as previously observed on tomato, T. urticae benefits from the suppression of bean defences when sharing a leaf with T. evansi. Phytohormone treatments revealed that the reproductive performance of both species decreases with artificially induced JA defences, irrespective of the presence of SA. We found that the molecular suppression and induction of defences is mostly, but not exclusively restricted to the leaf area from where the mites feed. In full leaves co-infested with both mites, levels of marker gene induction were comparable to the inducer mite T. urticae, although not as prominent, while in smaller feeding arenas where both species fed closely to each other, the expression of a JA-responsive proteinase inhibitor was suppressed. When residing alone on a leaf, both mites had distinct preferred feeding sites with only partial overlap, but when sharing a leaf, T. evansi retained its preferred feeding site and T. urticae moved away from its own. We argue that the suppression of defences by T. evansi is mostly, although not exclusively, locally restricted, and thus the spatial distribution of individuals on the leaf is a strong determinant of competitor facilitation. This suggests that traits that displace competitors from plant tissues with suppressed defences would be under selection to co-evolve together with defence suppression.

ecology↗

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↗

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↗

bioRxiv2020

Plant-derived CO2 mediates long-distance host location and quality assessment by a root herbivore

Insect herbivores can use volatile and visual cues to locate and select suitable host plants from a distance. The importance of CO2, arguable the most conserved volatile marker of metabolic activity, is not well understood in this context, even though many herbivores are known to respond to minute differences in CO2 concentrations. To address this gap of knowledge, we manipulated CO2 perception of the larvae of the western corn rootworm (Diabrotica virgifera virgifera; WCR) through RNA interference and studied how CO2 perception impacts their interaction with their host plant, maize (Zea mays). We show that the expression of a putative Group 2 carbon dioxide receptor, DvvGr2, is specifically required for dose-dependent larval responses to CO2 in the ppm range. Silencing DvvGr2 has no effect on the ability of WCR larvae to locate host plants at short distance (<9 cm), but impairs host location at greater distances. Using soil arenas and olfactometer experiments in combination with DvvGr2 silencing and CO2 scrubbing, we demonstrate that WCR larvae use CO2 as a long-range host plant finding cue, but employ other volatiles for short-range host location. We furthermore show that the larvae use CO2 as a fitness-relevant long-distance indicator of plant nutritional status: Maize plants that are well-fertilized emit more CO2 from their roots and are better hosts for WCR than plants that are nutrient-deficient, and the capacity of WCR larvae to distinguish between these plants depends exclusively on their capacity to perceive CO2 through DvvGr2. This study unravels how CO2 can mediate plant-herbivore interactions by serving as a distance-dependent host location and quality assessment cue.

ecology↗

bioRxiv2020

Tissue-specific volatile-mediated defense regulation in maize leaves and roots

O_LIPlant leaves that are exposed to herbivore induced plant volatiles (HIPVs) respond by increasing their defenses. Whether this phenomenon also occurs in the roots is unknown. C_LIO_LIUsing maize (Zea mays), whose leaves respond strongly to leaf HIPVs, we measured the impact of root HIPVs, emanating from plants infested by the banded cucumber beetle (Diabrotica balteata), on constitutive and herbivore-induced levels of root soluble sugars, starch, total soluble proteins, free amino acids, volatile and non-volatile secondary metabolites, defense gene expression, growth and root herbivore resistance of neighboring plants. C_LIO_LIHIPV exposure did not alter constitutive or induced levels of any of the measured root traits. Furthermore, HIPV exposure did not reduce the performance and survival of banded cucumber beetle larvae on maize or teosinte. Cross-exposure experiments revealed that maize roots, in contrast to maize leaves, neither emit nor respond strongly to defense-regulating HIPVs. C_LIO_LITogether, these results demonstrate that volatile-mediated defense regulation is restricted to the leaves of maize and teosinte, a finding which is in line with the lower diffusibility of volatiles in the soil and the availability of other, potentially more efficient information conduits below ground. C_LI

plant biology↗