Benjamin Delory

Root-emitted volatile organic compounds: can they mediate belowground plant-plant interactions?

BackgroundAboveground, plants release volatile organic compounds (VOCs) that act as chemical signals between neighbouring plants. It is now well documented that VOCs emitted by the roots in the plant rhizosphere also play important ecological roles in the soil ecosystem, notably in plant defence because they are involved in interactions between plants, phytophagous pests and organisms of the third trophic level. The roles played by root-emitted VOCs in between- and within-plant signalling, however, are still poorly documented in the scientific literature.ScopeGiven that (1) plants release volatile cues mediating plant-plant interactions aboveground, (2) roots can detect the chemical signals originating from their neighbours, and (3) roots release VOCs involved in biotic interactions belowground, the aim of this paper is to discuss the roles of VOCs in between- and within-plant signalling belowground. We also highlight the technical challenges associated with the analysis of root-emitted VOCs and the design of experiments targeting volatile-mediated root-root interactions.ConclusionsWe conclude that root-root interactions mediated by volatile cues deserve more research attention and that both the analytical tools and methods developed to study the ecological roles played by VOCs in interplant signalling aboveground can be adapted to focus on the roles played by root-emitted VOCs in between- and within-plant signalling.

The Importance of Being First: Exploring Priority and Diversity Effects in a Grassland Field Experiment

Diversity of species and order of arrival can have strong effects on ecosystem functioning and community composition, but these two have rarely been explicitly combined in experimental setups. We measured the effects of both species diversity and order of arrival on ecosystem function and community composition in a grassland field experiment, thus combining biodiversity and assembly approaches. We studied the effect of order of arrival of three plant functional groups (PFGs: grasses, legumes, and non-leguminous forbs) and of sowing low and high diversity seed mixtures (9 or 21 species) on species composition and aboveground biomass. The experiment was set up in two different soil types. Differences in PFG order of arrival affected the biomass, the number of species and community composition. As expected, we found higher aboveground biomass when sowing legumes before the other PFGs, but this effect was not continuous over time. We did not find a positive effect of sown diversity on aboveground biomass (even if it influenced species richness as expected). No interaction were found between the two studied factors. We found that sowing legumes first may be a good method for increasing productivity whilst maintaining diversity of central European grasslands, although the potential for long-lasting effects needs further study. In addition, the mechanisms behind the non-continuous priority effects we found need to be further researched, taking weather and plant-soil feedbacks into account.

archiDART: an R package for the automated computation of plant root architectural traits

Background and aimsIn order to analyse root system architectures (RSAs) from captured images, a variety of manual (e.g. Data Analysis of Root Tracings, DART), semi-automated and fully automated software packages have been developed. These tools offer complementary approaches to study RSAs and the use of the Root System Markup Language (RSML) to store RSA data makes the comparison of measurements obtained with different (semi-) automated root imaging platforms easier. The throughput of the data analysis process using exported RSA data, however, should benefit greatly from batch analysis in a generic data analysis environment (R software).MethodsWe developed an R package (archiDART) with five functions. It computes global RSA traits, root growth rates, root growth directions and trajectories, and lateral root distribution from DART-generated and/or RSML files. It also has specific plotting functions designed to visualise the dynamics of root system growth.ResultsThe results demonstrated the ability of the package’s functions to compute relevant traits for three contrasted RSAs (Brachypodium distachyon [L.] P. Beauv., Hevea brasiliensis Müll. Arg. and Solanum lycopersicum L.).ConclusionsThis work extends the DART software package and other image analysis tools supporting the RSML format, enabling users to easily calculate a number of RSA traits in a generic data analysis environment.

Foraging wireworms are attracted to root-produced volatile aldehydes

Soil-dwelling insects are known to react to chemical cues they encounter in the rhizosphere. Whether wireworms (Coleoptera, Elateridae) use root-emitted volatile organic chemicals to localize their host plant remains, however, poorly understood. Here, we aimed at identifying chemical cues released by barley roots that attract Agriotes sordidus. In a first behavioral experiment, we assessed the ability of wireworms to orient towards live barley roots, using dual-choice olfactometers suitable for belowground insects. Then, we collected the volatile organic compounds (VOC) produced by barley roots using a dynamic head-space sampling approach. VOC were quantified and identified using gas chromatography—mass spectrometry (GC–MS). The odorant blend is composed of four aldehydes, namely hexanal, (E)-hex-2-enal, (E)-non-2-enal, and (E,Z)-nona-2,6-dienal. In a second set of dual-choice bioassays, wireworms were attracted towards a synthetic blend of these four major compounds. However, the synthetic blend was not as attractive as live roots, which is partially explained by the absence of CO2, commonly known as a strong attractant for soil-dwelling insects. While CO2 indicates the presence of living material in the vicinity, we hypothesize that additional VOC inform about the plant suitability. A better understanding of these belowground signals would contribute to the development of new integrated control strategies against wireworms.

Priority effects caused by plant order of arrival affect below‐ground productivity

Plant species that arrive first in the system can affect assembly (priority effects). However, effects of order of arrival of different plant functional groups (PFGs) on root development have not yet been investigated under field conditions. We measured standing and fine root length density in the first and third year of a grassland field experiment. We wanted to know if manipulating PFG order of arrival would affect root development, and if priority effects are modulated by soil type. Sowing legumes first created a priority effect that was found in the first and third year, with a lower standing root length density in this treatment, even though the plant community composition was different in each of the studied years. Fine root length density was not affected by order of arrival, but changed according to the soil type. Synthesis. We found strong evidence that sowing legumes first created a priority effect below-ground that was found in the first and third year of this field experiment, even though the functional group dominance was different in each of the studied years.

Barley (Hordeum distichon L.) roots synthesise volatile aldehydes with a strong age-dependent pattern and release (E)-non-2-enal and (E,Z)-nona-2,6-dienal after mechanical injury

In the context of chemical ecology, the analysis of the temporal production pattern of volatile organic compounds (VOCs) in root tissues and the emission rate measurement of root-emitted VOCs are of major importance for setting up experiments to study the implication of these compounds in biotic interactions. Such analyses, however, remain challenging because of the belowground location of plant root systems. In this context, this study describes the evolution of the root VOC production pattern of barley (Hordeum distichon L.) at five developmental stages from germination to the end of tillering and evaluates the emission of the identified VOCs in an artificial soil. VOCs produced by crushed root tissues and released by unexcavated root systems were analysed using dynamic sampling devices coupled to a gas chromatography-mass spectrometry methodology (synchronous SCAN/SIM). The results showed that, at each analysed developmental stage, crushed barley roots produced mainly four volatile aldehydes: hexanal; (E)-hex-2-enal; (E)-non-2-enal; and (E,Z)-nona-2,6-dienal. Higher total and individual VOC concentrations were measured in 3-day-old seminal roots compared with older phenological stages. For each developmental stage, the lipoxygenase (LOX) activity was greater for linoleic acid than α-linolenic acid and the greatest LOX activities using linoleic and α-linolenic acids as substrates were measured in 7- and 3-day-old roots, respectively. The analysis of VOCs released by barley roots into the soil showed that (E)-non-2-enal and (E,Z)-nona-2,6-dienal were the only VOCs emitted in quantifiable amounts by mechanically injured roots.

Legacy effects of land-use modulate tree growth responses to climate extremes

Climate change can impact forest ecosystem processes via individual tree and community responses. While the importance of land-use legacies in modulating these processes have been increasingly recognised, evidence of former land-use mediated climate-growth relationships remain rare. We analysed how differences in former land-use (i.e. forest continuity) affect the growth response of European beech to climate extremes. Here, using dendrochronological and fine root data, we show that ancient forests (forests with a long forest continuity) and recent forests (forests afforested on former farmland) clearly differ with regard to climate–growth relationships. We found that sensitivity to climatic extremes was lower for trees growing in ancient forests, as reflected by significantly lower growth reductions during adverse climatic conditions. Fine root morphology also differed significantly between the former land-use types: on average, trees with high specific root length (SRL) and specific root area (SRA) and low root tissue density (RTD) were associated with recent forests, whereas the opposite traits were characteristic of ancient forests. Moreover, we found that trees of ancient forests hold a larger fine root system than trees of recent forests. Our results demonstrate that land-use legacy-mediated modifications in the size and morphology of the fine root system act as a mechanism in regulating drought resistance of beech, emphasising the need to consider the ‘ecological memory’ of forests when assessing or predicting the sensitivity of forest ecosystems to global environmental change.

archiDART v3.0: A new data analysis pipeline allowing the topological analysis of plant root systems

Quantifying plant morphology is a very challenging task that requires methods able to capture the geometry and topology of plant organs at various spatial scales. Recently, the use of persistent homology as a mathematical framework to quantify plant morphology has been successfully demonstrated for leaves, shoots, and root systems. In this paper, we present a new data analysis pipeline implemented in the R package archiDART to analyse root system architectures using persistent homology. In addition, we also show that both geometric and topological descriptors are necessary to accurately compare root systems and assess their natural complexity.

Plutella xylostella (L.) infestations at varying temperatures induce the emission of specific volatile blends by Arabidopsis thaliana (L.) Heynh

The effect of combined abiotic and biotic factors on plant volatile organic compound (VOC) emissions is poorly understood. This study evaluated the VOC emissions produced by Arabidopsis thaliana (L.) Col-0 subjected to 3 temperature regimes (17, 22, and 27°C) in the presence and absence of Plutella xylostella larvae over 2 time intervals (0–4 and 4–8 h), in comparison to control plants. The analyses of VOCs emitted by Arabidopsis plants were made by headspace solid phase microextraction (HS-SPME) coupled with gas chromatography-mass spectrometry (GC-MS). It was found that certain volatile groups (e.g., alcohols, ketones, aldehydes, and terpenes) are induced by both single factors (temperature or larval infestation) and combined factors (temperature and larvae interactions), whereas other volatile groups (e.g., isothiocyanates [ITCs] and nitrile) were specific to the experimental conditions. ITCs (mainly 4-methylpentyl isothiocyanate) were emitted from plants subjected to larval infestation at 17 and 27°C after the 2 time intervals. The proportions of sulfides (mainly dimethyl disulfide) and 4-(methylthio) butanenitrile were significantly higher on herbivore-infested plants at 22°C compared to the other treatments. Overall, our findings indicate that changes in all experimental conditions caused significant changes to the VOC emissions of Arabidopsis plants. Therefore, the interaction between temperature and larval feeding may represent an important factor determining the variability of volatile emissions by plants subjected to multiple simultaneous factors.

Interaction between the barley allelochemical compounds gramine and hordenine and artificial lipid bilayers mimicking the plant plasma membrane

Some plants affect the development of neighbouring plants by releasing secondary metabolites into their environment. This phenomenon is known as allelopathy and is a potential tool for weed management within the framework of sustainable agriculture. While many studies have investigated the mode of action of various allelochemicals (molecules emitted by allelopathic plants), little attention has been paid to their initial contact with the plant plasma membrane (PPM). In this paper, this key step is explored for two alkaloids, gramine and hordenine, that are allelochemicals from barley. Using in vitro bioassays, we first showed that gramine has a greater toxicity than hordenine towards a weed commonly found in northern countries (Matricaria recutita L.). Then, isothermal titration calorimetry was used to show that these alkaloids spontaneously interact with lipid bilayers that mimic the PPM. The greater impact of gramine on the thermotropic behaviour of lipids compared to hordenine was established by means of infrared spectroscopy. Finally, the molecular mechanisms of these interactions were explored with molecular dynamics simulations. The good correlation between phytotoxicity and the ability to disturb lipid bilayers is discussed. In this study, biophysical tools were used for the first time to investigate the interactions of allelochemicals with artificial PPM.