Systemic root signalling in a belowground, volatile-mediated tritrophic interaction

Plants attacked by leaf herbivores release volatile organic compounds (VOCs) both locally from the wounded site and systemically from non-attacked tissues. These volatiles serve as attractants for predators and parasitoids. This phenomenon is well described for plant leaves, but systemic induction of VOCs in the roots has remained unstudied. We assessed the spatial and temporal activation of the synthesis and release of (E)-β-caryophyllene (EβC) in maize roots upon feeding by larvae of Diabrotica virgifera virgifera, as well as the importance of systemically produced EβC for the attraction of the entomopathogenic nematode Heterorhabditis megidis. The production of EβC was found to be significantly stronger at the site of attack than in non-attacked tissues. A weak, but significant, increase in transcriptional activity of the EβC synthase gene tps23 and a corresponding increase in EβC content were observed in the roots above the feeding site and in adjacent roots, demonstrating for the first time that herbivory triggers systemic production of a volatile within root systems. In belowground olfactometers, the nematodes were significantly more attracted towards local feeding sites than systemically induced roots. The possible advantages and disadvantages of systemic volatile signalling in roots are discussed

Metabolization and sequestration of plant specialized metabolites in insect herbivores: Current and emerging approaches.

Herbivorous insects encounter diverse plant specialized metabolites (PSMs) in their diet, that have deterrent, anti-nutritional, or toxic properties. Understanding how they cope with PSMs is crucial to understand their biology, population dynamics, and evolution. This review summarizes current and emerging cutting-edge methods that can be used to characterize the metabolic fate of PSMs, from ingestion to excretion or sequestration. It further emphasizes a workflow that enables not only to study PSM metabolism at different scales, but also to tackle and validate the genetic and biochemical mechanisms involved in PSM resistance by herbivores. This review thus aims at facilitating research on PSM-mediated plant-herbivore interactions

Metabolization and sequestration of plant specialized metabolites in insect herbivores: Current and emerging approaches

Herbivorous insects encounter diverse plant specialized metabolites (PSMs) in their diet, that have deterrent, anti-nutritional, or toxic properties. Understanding how they cope with PSMs is crucial to understand their biology, population dynamics, and evolution. This review summarizes current and emerging cutting-edge methods that can be used to characterize the metabolic fate of PSMs, from ingestion to excretion or sequestration. It further emphasizes a workflow that enables not only to study PSM metabolism at different scales, but also to tackle and validate the genetic and biochemical mechanisms involved in PSM resistance by herbivores. This review thus aims at facilitating research on PSM-mediated plant-herbivore interactions

The Chemical Ecology of Benzoxazinoids

Benzoxazinoids are specialized metabolites that modulate plant physiology and plant interactions with their environment. In this review, we synthesize their multiple functions and ecological relevance. We first provide an overview of benzoxazinoid biosynthesis and highlight known regulatory elements involved in modulating their production. We then outline the role of benzoxazinoids in plant nutrition, vegetative and reproductive growth, and defense. We further summarize benzoxazinoid response to environmental factors such as temperature, drought, CO2, light, or nutrient levels and emphasize their potential role in tolerating abiotic stresses. Finally, we argue that benzoxazinoids act as a strong selective force on different trophic levels by shaping the plant interactions with microbes, insect herbivores, and competitor plants. Understanding the pivotal role of benzoxazinoids in plant biology is crucial to apprehend their impact on (agro)ecosystem functioning and diversity

Chemical host-seeking cues of entomopathogenic nematodes

Entomopathogenic nematodes (EPNs) are obligate parasites that infect a broad range of insect species. Host-seeking is a crucial step for EPN infection success and survival. Yet, the identity and ecological functions of chemicals involved in host-seeking by EPNs remain overlooked. In this review, we report known CO2, plant-derived and insect-derived cues shaping EPN host-seeking and recognition. Despite species-specific response to environmental cues, we highlight a hierarchical integration of chemicals by EPNs. We further emphasize the impact of EPN selection pressure, age, and experience on their responsiveness to infochemicals. Finally, we feature that EPN chemical ecology can translate into powerful sustainable strategies to control insect herbivores in agriculture

Using plant chemistry to improve interactions between plants, herbivores and their natural enemies: challenges and opportunities

Plant secondary (or specialized) metabolites determine multitrophic interaction dynamics. Herbivore natural enemies exploit plant volatiles for host location and are negatively affected by plant defense chemicals that are transferred through herbivores. Recent work shows that herbivore natural enemies can evolve resistance to plant defense chemicals, and that generating plant defense resistance through forward evolution enhances their capacity to prey on herbivores. Here, we discuss how this knowledge can be used to engineer better biocontrol agents. We argue that herbivore natural enemies which are adapted to plant chemistry will likely enhance the efficacy of future pest control efforts. Detailed phenotyping and field experiments will be necessary to quantify costs and benefits of optimizing chemical links between plants and higher trophic levels

Using plant chemistry to improve interactions between plants, herbivores and their natural enemies: challenges and opportunities

Plant secondary (or specialized) metabolites determine multitrophic interaction dynamics. Herbivore natural enemies exploit plant volatiles for host location and are negatively affected by plant defense chemicals that are transferred through herbivores. Recent work shows that herbivore natural enemies can evolve resistance to plant defense chemicals, and that generating plant defense resistance through forward evolution enhances their capacity to prey on herbivores. Here, we discuss how this knowledge can be used to engineer better biocontrol agents. We argue that herbivore natural enemies which are adapted to plant chemistry will likely enhance the efficacy of future pest control efforts. Detailed phenotyping and field experiments will be necessary to quantify costs and benefits of optimizing chemical links between plants and higher trophic levels

Sequence of arrival determines plant-mediated interactions between herbivores

1. Induced changes in plant quality can mediate indirect interactions between herbivores. Although the sequence of attack by different herbivores has been shown to influence plant responses, little is known about how this affects the herbivores themselves. 2. We therefore investigated how induction by the leaf herbivore Spodoptera frugiperda influences resistance of teosinte (Zea mays mexicana) and cultivated maize (Zea mays mays) against root-feeding larvae of Diabrotica virgifera virgifera. The importance of the sequence of arrival was tested in the field and laboratory. 3. Spodoptera frugiperda infestation had a significant negative effect on colonization by D. virgifera larvae in the field and weight gain in the laboratory, but only when S. frugiperda arrived on the plant before the root herbivore. When S. frugiperda arrived after the root herbivore had established, no negative effects on larval performance were detected. Yet, adult emergence of D. virgifera was reduced even when the root feeder had established first, indicating that the negative effects were not entirely absent in this treatment. 4. The defoliation of the plants was not a decisive factor for the negative effects on root herbivore development, as both minor and major leaf damage resulted in an increase in root resistance and the extent of biomass removal was not correlated with root-herbivore growth. We propose that leaf-herbivore-induced increases in feeding-deterrent and/or toxic secondary metabolites may account for the sequence-specific reduction in root-herbivore performance. 5. Synthesis. Our results demonstrate that the sequence of arrival can be an important determinant of plant-mediated interactions between insect herbivores in both wild and cultivated plants. Arriving early on a plant may be an important strategy of insects to avoid competition with other herbivores. To fully understand plant-mediated interactions between insect herbivores, the sequence of arrival should be taken into account

Isolation and Structure Determination of Drought-Induced Multihexose Benzoxazinoids from Maize (Zea mays).

Benzoxazinoids (BXDs) are plant specialized metabolites exerting a pivotal role in plant nutrition, allelopathy, and defenses. Multihexose benzoxazinoids were previously observed in cereal-based food products such as whole-grain bread. However, their production in plants and exact structure have not been fully elucidated. In this study, we showed that drought induced the production of di-, tri-, and even tetrahexose BXDs in maize roots and leaves. We performed an extensive nuclear magnetic resonance study and elucidated the nature and linkage of the sugar units, which were identified as gentiobiose units β-linked (1″ → 6') for the dihexoses and (1″ → 6')/(1‴ → 6″) for the trihexoses. Drought induced the production of DIMBOA-2Glc, DIMBOA-3Glc, HMBOA-2Glc, HMBOA-3Glc, and HDMBOA-2Glc. The induction was common among several maize lines and the strongest in seven-day-old seedlings. This work provides ground to further characterize the BXD synthetic pathway, its relevance in maize-environment interactions, and its impact on human health