Root Exudation of Specialized Molecules for Plant-Environment Interaction

It has been estimated that between 40 and 60 % of the assimilated carbon is diverted to the roots and released in the rhizosphere in form of root exudates. Root exudates thus define a complex mixture of low and high molecular weight compounds, including carbohydrates, amino acids, organic, and proteins, but also a broad spectrum of specialized molecules, such as flavonoids, glucosinolates, terpenoids, or alkaloids. Root exudates favour soil mineral nutrition, can bind to soil aggregate and in turn modify soil physico-chemical properties, but also mediate plant-plant, plant-microbe, and plant-animal interactions belowground. With this review, we aim to highlight how chemical ecologists have approached the study of root exudates-mediated interactions between plants and their biotic and abiotic surroundings. We do so by presenting a series of study cases for, on one hand, showcasing different methodologies that have been developed to test the activity of different root exudates, and, on the other hand, to show the broad array of interactions mediated by root exudates. Ultimately, we aim to spur further research and collaborations between chemists and ecologists studying belowground chemically-mediated interactions, so as to tackle essential challenges in terms of food security and climate change in the near future

Belowground Chemical Signaling in Maize: When Simplicity Rhymes with Efficiency

Maize roots respond to feeding by larvae of the beetle Diabrotica virgifera virgifera by releasing (E)-β-caryophyllene. This sesquiterpene, which is not found in healthy maize roots, attracts the entomopathogenic nematode Heterorhabditis megidis. In sharp contrast to the emission of virtually only this single compound by damaged roots, maize leaves emit a blend of numerous volatile organic compounds in response to herbivory. To try to explain this difference between roots and leaves, we studied the diffusion properties of various maize volatiles in sand and soil. The best diffusing compounds were found to be terpenes. Only one other sesquiterpene known for maize, α-copaene, diffused better than (E)-β-caryophyllene, but biosynthesis of the former is far more costly for the plant than the latter. The diffusion of (E)-β-caryophyllene occurs through the gaseous rather than the aqueous phase, as it was found to diffuse faster and further at low moisture level. However, a water layer is needed to prevent complete loss through vertical diffusion, as was found for totally dry sand. Hence, it appears that maize has adapted to emit a readily diffusing and cost-effective belowground signal from its insect-damaged root

The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes

Background: Entomopathogenic nematodes (EPNs) are tiny parasitic worms that parasitize insects, in which they reproduce. Their foraging behavior has been subject to numerous studies, most of which have proposed that, at short distances, EPNs use chemicals that are emitted directly from the host as host location cues. Carbon dioxide (CO2) in particular has been implicated as an important cue. Recent evidence shows that at longer distances several EPNs take advantage of volatiles that are specifically emitted by roots in response to insect attack. Studies that have revealed these plant-mediated interactions among three trophic levels have been met with some disbelief. Scope: This review aims to take away this skepticism by summarizing the evidence for a role of root volatiles as foraging cues for EPNs. To reinforce our argument, we conducted olfactometer assays in which we directly compared the attraction of an EPN species to CO2 and two typical inducible root volatiles. Conclusions: The combination of the ubiquitous gas and a more specific root volatile was found to be considerably more attractive than one of the two alone. Hence, future studies on EPN foraging behavior should take into account that CO2 and plant volatiles may work in synergy as attractants for EPNs. Recent research efforts also reveal prospects of exploiting plant-produced signals to improve the biological control of insect pests in the rhizospher

The dual effects of root-cap exudates on nematodes: from quiescence in plant-parasitic nematodes to frenzy in entomopathogenic nematodes

Plant defences against root antagonists invigorate root protagonists. The same root-cap exudate impairs the mobility of plant-parasitic nematodes and increases the performances of insect-killing nematode

Capsules containing entomopathogenic nematodes as a Trojan horse approach to control the western corn rootworm

Aims: The use of entomopathogenic nematodes in the biological control of soil insect pests is hampered by the costly and inadequate application techniques. As a possible solution we evaluated a nematode encapsulation approach that offers effective application and may possibly attract the pest by adding attractants to the capsule shell. Methods: Heterorhabditis bacteriophora nematodes, which show high virulence against the maize root pest Diabrotica virgifera virgifera, were encapsulated in a polysaccharide shell derived from the algae Laminaria ssp. Shells of varying thickness and composition were evaluated. Results: Nematodes readily survived the encapsulation process and were able, varying with shell thickness and temperature, to break through the shell and subsequently infect hosts. The added attractants and feeding stimulants to the shell attracted the pest larvae as much as maize roots. In field trials, encapsulated H. bacteriophora nematodes were more effective in controlling D. v. virgifera than those sprayed in water over the soil surface, but in these trials the addition of stimulants did not increase the control efficiency. Conclusions: The study demonstrates that nematodes can be successfully applied in capsules in the field. Further improvements are needed to make the capsules a cost effective alternative to conventional field application of nematode

How maize root volatiles affect the efficacy of entomopathogenic nematodes in controlling the western corn rootworm?

Because the ferocious maize pest Diabrotica virgifera virgifera LeConte can adapt to all currently used control strategies, focus has turned to the development of novel, more sustainable control methods, such as biological control using entomopathogenic nematodes (EPN). A good understanding of the biology and behaviour of these potential control agents is essential for their successful deployment. Root systems of many maize varieties emit (E)-β-caryophyllene (EβC) in response to feeding by larvae of the beetle D. v. virgifera. This sesquiterpene has been shown to attract certain species of EPN, thereby enhancing their control potential. In this study, we tested the effect of this root-produced volatile on the field efficacy of the three EPN Heterorhabditis bacteriophora, Heterorhabditis megidis and Steinernema feltiae against D. v. virgifera larvae in southern Hungary. By comparing beetle emergence and root damage for two maize varieties, one that emits EβC and one that does not, it was found that root protection by H. megidis and S. feltiae was higher on the emitting variety, but this was not the case for H. bacteriophora. Overall, all three nematode species showed good control potential. We conclude that, if properly applied and in combination with the right maize variety, the release of these nematodes can be as effective as other control method

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

Root herbivore performance suppressed when feeding on a jasmonate-induced pasture grass

1. Plants defend themselves from insect herbivore attack using a range of physical and chemical defences which are in many cases regulated by phytohormones such as jasmonates. While much more is known about how jasmonates regulate defence against above‐ground herbivores (e.g. herbivores of leaves), there is increasing interest in how they influence below‐ground defences. 2. For the Poaceae, most below‐ground studies focus on highly domesticated cereals. Here it is demonstrated how exogenous application of methyl jasmonate (MeJA) to the leaf blades of a non‐domesticated pasture grass (Microlaena stipoides) caused a more than two‐fold decrease in relative growth rate (RGR) of a root‐feeding chafer (Dermolepida albohirtum). MeJA treatment did not affect root consumption rates, but substantially reduced the efficiency of conversion of ingested food to body mass. 3. Non‐targeted metabolomics identified significant changes in the metabolome of MeJA‐induced plants, with three compounds (a galactolipid, a trihydroxy fatty acid and a lysophospholipid) found to be correlated with herbivore RGR, although their roles in herbivore defence remain uncertain. 4. This study suggests that an important Australian pasture grass can become better defended against root herbivores via enhanced jasmonate activity

Root responses to domestication, precipitation and silicification: weeping meadow grass simplifies and alters toughness

Background and aims Plant breeding usually focuses on conspicuous above-ground plant traits, yet roots fundamentally underpin plant fitness. Roots show phenotypic plasticity in response to soil conditions but it is unclear whether domesticated plants respond like their ancestors. We aimed to determine how root traits differed between ancestral and domesticated types of a meadow grass (Microlaena stipoides) under altered regimes of precipitation and soil silicon availability. Methods We subjected the two grass types to three simulated precipitation regimes (ambient, +50%/deluge and −50%/drought) in soil with (Si+) and without (Si−) silicon supplementation and then characterised root biomass, architectural complexity and toughness in addition to shoot traits. Results Domestication increased root tissue density, decreased specific root length (SRL) and decreased root architectural complexity. Domestication also increased root strength under Si− conditions but not Si+ conditions. Fine roots, SRL, architectural complexity and the force required to tear the roots all decreased under deluge. The ancestral and domesticated grasses responded similarly to precipitation, except that the latter had weaker roots (decreased fracture strain) under drought. Conclusions Domestication and increased precipitation caused changes in M. stipoides root traits that could be beneficial against some stresses (e.g. soil compaction, herbivory) but not others (e.g. drought)