Root-exuded specialized metabolites reduce arsenic toxicity in maize.

By releasing specialized metabolites, plants modify their environment. Whether and how specialized metabolites protect plants against toxic levels of trace elements is not well understood. We evaluated whether benzoxazinoids, which are released into the soil by major cereals, can confer protection against arsenic toxicity. Benzoxazinoid-producing maize plants performed better in arsenic-contaminated soils than benzoxazinoid-deficient mutants in the greenhouse and the field. Adding benzoxazinoids to the soil restored the protective effect, and the effect persisted to the next crop generation via positive plant-soil feedback. Arsenate levels in the soil and total arsenic levels in the roots were lower in the presence of benzoxazinoids. Thus, the protective effect of benzoxazinoids is likely soil-mediated and includes changes in soil arsenic speciation and root accumulation. We conclude that exuded specialized metabolites can enhance protection against toxic trace elements via soil-mediated processes and may thereby stabilize crop productivity in polluted agroecosystems.

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 (BXs), the dominant specialized and bioactive metabolites in the root exudates of maize plants. In vitro experiments revealed that BXs 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 BXs better compared to nonhost 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 BX-exuding maize roots. Thus, strain-dependent tolerance to BXs 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 root-derived antimicrobial compounds is an underlying mechanism determining the structure of host-specific microbial communities.

Far-red light increases maize volatile emissions in response to volatile cues from neighbouring plants.

Plants perceive the presence and defence status of their neighbours through light and volatile cues, but how plants integrate both stimuli is poorly understood. We investigated if and how low Red to Far red light (R:FR) ratios, indicative of shading or canopy closure, affect maize (Zea mays) responses to herbivore-induced plant volatiles (HIPVs), including the green leaf volatile (Z)-3-hexenyl acetate. We modulated light signalling and perception by using FR supplementation and a phyB1phyB2 mutant, and we determined volatile release as a response readout. To gain mechanistic insights, we examined expression of volatile biosynthesis genes, hormone accumulation, and photosynthesis. Exposure to a full blend of HIPVs or (Z)-3-hexenyl acetate induced maize volatile release. Short-term FR supplementation increased this response. In contrast, prolonged FR supplementation or constitutive phytochrome B inactivation in phyB1phyB2 plants showed the opposite response. Short-term FR supplementation enhanced photosynthesis and stomatal conductance and (Z)-3-hexenyl acetate-induced JA-Ile levels. We conclude that a FR-enriched light environment can prompt maize plants to respond more strongly to HIPVs emitted by neighbours, which might be explained by changes in photosynthetic processes and phytochrome B signalling. Our findings reveal interactive responses to light and volatile cues with potentially important consequences for plant-plant and plant-herbivore interactions.

Volatile-mediated oviposition preference for healthy over root-infested plants by the European corn borer.

The selection of oviposition sites by female moths is crucial in shaping their progeny performance and survival, and consequently in determining insect fitness. Selecting suitable plants that promote the performance of the progeny is referred to as the Preference-Performance hypothesis (or 'mother-knows-best'). While root infestation generally reduces the performance of leaf herbivores, little is known about its impact on female oviposition. We investigated whether maize root infestation by the Western corn rootworm (WCR) affects the oviposition preference and larval performance of the European corn borer (ECB). ECB females used leaf volatiles to select healthy plants over WCR-infested plants. Undecane, a compound absent from the volatile bouquet of healthy plants, was the sole compound to be upregulated upon root infestation and acted as a repellent for first oviposition. ECB larvae yet performed better on plants infested below-ground than on healthy plants, suggesting an example of 'bad motherhood'. The increased ECB performance on WCR-infested plants was mirrored by an increased leaf consumption, and no changes in the plant primary or secondary metabolism were detected. Understanding plant-mediated interactions between above- and below-ground herbivores may help to predict oviposition decisions, and ultimately, to manage pest outbreaks in the field.

The plant metabolome guides fitness-relevant foraging decisions of 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 combine and 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 combined mediators of short-distance host finding and acceptance. While sugars improve the capacity of rootworm larvae to find a host plant and to distinguish postembryonic 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 postembryonic 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 combination 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.

Effects of lexical skills and orthographic neighborhood size in word memory.

Two experiments were designed to investigate the relationship between individual lexical skills in young adults and memory performance on words varying by their orthographic neighborhood size. In Experiment 1, a sample of 100 university students were administrated a set of spelling, reading, and vocabulary tests to assess their lexical skills. Then, they had to learn mixed lists of words from high and low neighborhood size and perform free recall and memory recognition tasks. Importantly, high lexical skills were found to enhance free recall and, to a lesser extent, recognition. In addition, a typical mirror effect of neighborhood size was found in recognition as words were better recognized and also produced less false alarms when they had a low neighborhood size. In Experiment 2, pure lists of words were designed and a new sample of 90 university students was assessed. We replicated the effect of lexical skills in free recall and the effect of neighborhood size for hits in recognition. Spelling skills were found to interact with neighborhood size in free recall in that low spelling skills were associated with a facilitatory effect of neighborhood size. In recognition, a relation between reading skills and neighborhood size was found such that the higher the reading skills, the higher was the inhibitory effect of neighborhood size. These results provide new evidence of an influence of lexical skills in word memory performance and underline the role of orthographic neighborhood size in episodic memory tasks.

Soil chemistry determines whether defensive plant secondary metabolites promote or suppress herbivore growth.

Plant secondary (or specialized) metabolites mediate important interactions in both the rhizosphere and the phyllosphere. If and how such compartmentalized functions interact to determine plant-environment interactions is not well understood. Here, we investigated how the dual role of maize benzoxazinoids as leaf defenses and root siderophores shapes the interaction between maize and a major global insect pest, the fall armyworm. We find that benzoxazinoids suppress fall armyworm growth when plants are grown in soils with very low available iron but enhance growth in soils with higher available iron. Manipulation experiments confirm that benzoxazinoids suppress herbivore growth under iron-deficient conditions and in the presence of chelated iron but enhance herbivore growth in the presence of free iron in the growth medium. This reversal of the protective effect of benzoxazinoids is not associated with major changes in plant primary metabolism. Plant defense activation is modulated by the interplay between soil iron and benzoxazinoids but does not explain fall armyworm performance. Instead, increased iron supply to the fall armyworm by benzoxazinoids in the presence of free iron enhances larval performance. This work identifies soil chemistry as a decisive factor for the impact of plant secondary metabolites on herbivore growth. It also demonstrates how the multifunctionality of plant secondary metabolites drives interactions between abiotic and biotic factors, with potential consequences for plant resistance in variable environments.

Trade-offs between the accumulation of cuticular wax and jasmonic acid-mediated herbivory resistance in maize.

Plants have evolved complex physical and chemical defense systems that allow them to withstand herbivory infestation. Composed of a complex mixture of very-long-chain fatty acids (VLCFAs) and their derivatives, cuticular wax constitutes the first physical line of defense against herbivores. Here, we report the function of Glossy 8 (ZmGL8), which encodes a 3-ketoacyl reductase belonging to the fatty acid elongase complex, in orchestrating wax production and jasmonic acid (JA)-mediated defenses against herbivores in maize (Zea mays). The mutation of GL8 enhanced chemical defenses by activating the JA-dependent pathway. We observed a trade-off between wax accumulation and JA levels across maize glossy mutants and 24 globally collected maize inbred lines. In addition, we demonstrated that mutants defective in cuticular wax biosynthesis in Arabidopsis thaliana and maize exhibit enhanced chemical defenses. Comprehensive transcriptomic and lipidomic analyses indicated that the gl8 mutant confers chemical resistance to herbivores by remodeling VLCFA-related lipid metabolism and subsequent JA biosynthesis and signaling. These results suggest that VLCFA-related lipid metabolism has a critical role in regulating the trade-offs between cuticular wax and JA-mediated chemical defenses.

Water availability and plant-herbivore interactions.

Water is essential to plant growth and drives plant evolution and interactions with other organisms such as herbivores. However, water availability fluctuates, and these fluctuations are intensified by climate change. How plant water availability influences plant-herbivore interactions in the future is an important question in basic and applied ecology. Here we summarize and synthesize the recent discoveries on the impact of water availability on plant antiherbivore defense ecology and the underlying physiological processes. Water deficit tends to enhance plant resistance and escape traits (i.e. early phenology) against herbivory but negatively affects other defense strategies, including indirect defense and tolerance. However, exceptions are sometimes observed in specific plant-herbivore species pairs. We discuss the effect of water availability on species interactions associated with plants and herbivores from individual to community levels and how these interactions drive plant evolution. Although water stress and many other abiotic stresses are predicted to increase in intensity and frequency due to climate change, we identify a significant lack of study on the interactive impact of additional abiotic stressors on water-plant-herbivore interactions. This review summarizes critical knowledge gaps and informs possible future research directions in water-plant-herbivore interactions.

Stress tolerance in entomopathogenic nematodes: Engineering superior nematodes for precision agriculture.

Entomopathogenic nematodes (EPNs) are soil-dwelling parasitic roundworms commonly used as biocontrol agents of insect pests in agriculture. EPN dauer juveniles locate and infect a host in which they will grow and multiply until resource depletion. During their free-living stage, EPNs face a series of internal and environmental stresses. Their ability to overcome these challenges is crucial to determine their infection success and survival. In this review, we provide a comprehensive overview of EPN response to stresses associated with starvation, low/elevated temperatures, desiccation, osmotic stress, hypoxia, and ultra-violet light. We further report EPN defense strategies to cope with biotic stressors such as viruses, bacteria, fungi, and predatory insects. By comparing the genetic and biochemical basis of these strategies to the nematode model Caenorhabditis elegans, we provide new avenues and targets to select and engineer precision nematodes adapted to specific field conditions.

Natural adaptation and human selection of northeast African sheep genomes.

African sheep manifest diverse but distinct physio-anatomical traits, which are the outcomes of natural- and human-driven selection. Here, we generated 34.8 million variants from 150 indigenous northeast African sheep genomes sequenced at an average depth of ∼54× for 130 samples (Ethiopia, Libya) and ∼20× for 20 samples (Sudan). These represented sheep from diverse environments, tail morphology and post-Neolithic introductions to Africa. Phylogenetic and model-based admixture analysis provided evidence of four genetic groups corresponding to altitudinal geographic origins, tail morphotypes and possible historical introduction and dispersal of the species into and across the continent. Running admixture at higher levels of K (6 ≤ K ≤ 25), revealed cryptic levels of genome intermixing as well as distinct genetic backgrounds in some populations. Comparative genomic analysis identified targets of selection that spanned conserved haplotype structures overlapping clusters of genes and gene families. These were related to hypoxia responses, ear morphology, caudal vertebrae and tail skeleton length, and tail fat-depot structures. Our findings provide novel insights underpinning morphological variation and response to human-driven selection and environmental adaptation in African indigenous sheep.

Climate warming can reduce biocontrol efficacy and promote plant invasion due to both genetic and transient metabolomic changes.

Climate change may affect plant-herbivore interactions and their associated ecosystem functions. In an experimental evolution approach, we subjected replicated populations of the invasive Ambrosia artemisiifolia to a combination of simulated warming and herbivory by a potential biocontrol beetle. We tracked genomic and metabolomic changes across generations in field populations and assessed plant offspring phenotypes in a common environment. Using an integrated Bayesian model, we show that increased offspring biomass in response to warming arose through changes in the genetic composition of populations. In contrast, increased resistance to herbivory arose through a shift in plant metabolomic profiles without genetic changes, most likely by transgenerational induction of defences. Importantly, while increased resistance was costly at ambient temperatures, warming removed this constraint and favoured both vigorous and better defended plants under biocontrol. Climate warming may thus decrease biocontrol efficiency and promote Ambrosia invasion, with potentially serious economic and health consequences.

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 sometimes 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 y are behaviorally and metabolically resistant to sequestered benzoxazinoids and more infective toward 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 5 generations results in higher behavioral and metabolic resistance and benzoxazinoid-dependent infectivity toward 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 toward 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 potential target for the improvement of biological control agents.

Word imageability influences the emotionality effect in episodic memory.

This study examines how and to what extent imageability influences the effect of word emotionality in episodic memory. A total of 52 young adults successively performed a free recall task and a recognition task in which word emotionality and imageability were orthogonally manipulated across six conditions of French words: low-imageability positive words (e.g., éloge [praise]), low-imageability negative words (e.g., viral [viral]), low-imageability neutral words (e.g., global [global]), high-imageability positive words (e.g., ourson [teddy]), high-imageability negative words (e.g., tornade [tornado]), and low-imageability neutral words (e.g., noyau [core]). The results from both the recall and the recognition memory tasks show that word imageability enhances memory performance. Importantly, word imageability interacted with word emotionality in both tasks. Specifically, we found that the advantage of emotional over neutral words in episodic memory performance emerged for high-imageability words only, as did the advantage of positive over negative words. These results highlight the role of imageability in the mechanisms underlying emotional word episodic memory.

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.

Age-related evaluations of imageability and subjective frequency for 1286 neutral and emotional French words: ratings by young, middle-aged, and older adults.

This study aimed at providing imageability and subjective frequency ratings collected from four adult age groups ranging from 18 to 85 years old (18-25; 26-39; 40-59; and 60 and over) for 1286 neutral and emotional French words available in the EMA database (Gobin et al., 2017). Overall, the older adults rated words as more (subjectively) frequent and more imageable than the younger adults. Furthermore, we examined the relationships between subjective frequency and imageability, as well as those with emotional variables (i.e., valence, arousal) already available for these words, for each age group. For all age groups, more subjective frequent words were more imageable. Emotional words were more imageable and more frequent. Arousal scores were lower for low- and high-imageability words, and higher for more subjective frequent words. The strength of these links between subjective frequency, imageability, and emotional ratings was found to decrease as a function of age. Finally, by using the lexical decision reaction times and accuracy rates of young adults from Megalex (Ferrand et al., 2018), imageability and subjective frequency across age were found to provide an additional contribution to visual word recognition performance as compared to objective lexical variables (i.e., number of letters, syllables, objective frequency, orthographic neighborhood). More importantly, subjective frequency and imageability ratings from the youngest group predicted reaction times and accuracy better than ratings from the oldest group. By providing new age-adapted word characteristics, this norm should be of great use to researchers in the field of cognitive aging who use word materials.

ZEITLUPE facilitates the rhythmic movements of Nicotiana attenuata flowers.

Circadian organ movements are ubiquitous in plants. These rhythmic outputs are thought to be regulated by the circadian clock and auxin signalling, but the underlying mechanisms have not been clarified. Flowers of Nicotiana attenuata change their orientation during the daytime through a 140° arc to balance the need for pollinators and the protection of their reproductive organs. This rhythmic trait is under the control of the circadian clock and results from bending and re-straightening movements of the pedicel, stems that connect flowers to the inflorescence. Using an explant system that allowed pedicel growth and curvature responses to be characterized with high spatial and temporal resolution, we demonstrated that this movement is organ autonomous and mediated by auxin. Changes in the growth curvature of the pedicel are accompanied by an auxin gradient and dorsiventral asymmetry in auxin-dependent transcriptional responses; application of auxin transport inhibitors influenced the normal movements of this organ. Silencing the expression of the circadian clock component ZEITLUPE (ZTL) arrested changes in the growth curvature of the pedicel and altered auxin signalling and responses. IAA19-like, an Aux/IAA transcriptional repressor that is circadian regulated and differentially expressed between opposite tissues of the pedicel, and therefore possibly involved in the regulation of changes in organ curvature, physically interacted with ZTL. Together, these results are consistent with a direct link between the circadian clock and the auxin signalling pathway in the regulation of this rhythmic floral movement.

Marasmius oreades agglutinin enhances resistance of Arabidopsis against plant-parasitic nematodes and a herbivorous insect.

BACKGROUND: Plant-parasitic nematodes and herbivorous insects have a significant negative impact on global crop production. A successful approach to protect crops from these pests is the in planta expression of nematotoxic or entomotoxic proteins such as crystal proteins from Bacillus thuringiensis (Bt) or plant lectins. However, the efficacy of this approach is threatened by emergence of resistance in nematode and insect populations to these proteins. To solve this problem, novel nematotoxic and entomotoxic proteins are needed. During the last two decades, several cytoplasmic lectins from mushrooms with nematicidal and insecticidal activity have been characterized. In this study, we tested the potential of Marasmius oreades agglutinin (MOA) to furnish Arabidopsis plants with resistance towards three economically important crop pests: the two plant-parasitic nematodes Heterodera schachtii and Meloidogyne incognita and the herbivorous diamondback moth Plutella xylostella. RESULTS: The expression of MOA does not affect plant growth under axenic conditions which is an essential parameter in the engineering of genetically modified crops. The transgenic Arabidopsis lines showed nearly complete resistance to H. schachtii, in that the number of female and male nematodes per cm root was reduced by 86-91 % and 43-93 % compared to WT, respectively. M. incognita proved to be less susceptible to the MOA protein in that 18-25 % and 26-35 % less galls and nematode egg masses, respectively, were observed in the transgenic lines. Larvae of the herbivorous P. xylostella foraging on MOA-expression lines showed a lower relative mass gain (22-38 %) and survival rate (15-24 %) than those feeding on WT plants. CONCLUSIONS: The results of our in planta experiments reveal a robust nematicidal and insecticidal activity of the fungal lectin MOA against important agricultural pests which may be exploited for crop protection.

Herbivore-induced plant volatiles mediate defense regulation in maize leaves but not in maize roots.

Plant leaves that are exposed to herbivore-induced plant volatiles (HIPVs) respond by increasing their defenses, a phenomenon referred to as priming. Whether this phenomenon also occurs in the roots is unknown. Using maize plants, Zea mays, whose leaves respond strongly to leaf HIPVs, we measured the impact of belowground HIPVs, emanating from roots infested by the banded cucumber beetle, Diabrotica balteata, on constitutive and herbivore-induced levels of defense-related gene expression, phytohormones, volatile and non-volatile primary and secondary metabolites, growth and herbivore resistance in roots of neighbouring plants. HIPV exposure did not increase constitutive or induced levels of any of the measured root traits. Furthermore, HIPV exposure did not reduce the performance or survival of D. balteata on maize or its ancestor teosinte. Cross-exposure experiments between HIPVs from roots and leaves revealed that maize roots, in contrast to maize leaves, neither emit nor respond strongly to defense-regulating HIPVs. Together, these results demonstrate that volatile-mediated defense regulation is restricted to the leaves of maize. This finding is in line with the lower diffusibility of volatiles in the soil and the availability of other, potentially more efficient, information conduits below ground.

Climate Change Modulates Multitrophic Interactions Between Maize, A Root Herbivore, and Its Enemies.

How climate change will modify belowground tritrophic interactions is poorly understood, despite their importance for agricultural productivity. Here, we manipulated the three major abiotic factors associated with climate change (atmospheric CO2, temperature, and soil moisture) and investigated their individual and joint effects on the interaction between maize, the banded cucumber beetle (Diabrotica balteata), and the entomopathogenic nematode (EPN) Heterorhabditis bacteriophora. Changes in individual abiotic parameters had a strong influence on plant biomass, leaf wilting, sugar concentrations, protein levels, and benzoxazinoid contents. Yet, when combined to simulate a predicted climate scenario (Representative Concentration Pathway 8.5, RCP 8.5), their effects mostly counter-balanced each other. Only the sharp negative impact of drought on leaf wilting was not fully compensated. In both current and predicted scenarios, root damage resulted in increased leaf wilting, reduced root biomass, and reconfigured the plant sugar metabolism. Single climatic variables modulated the herbivore performance and survival in an additive manner, although slight interactions were also observed. Increased temperature and CO2 levels both enhanced the performance of the insect, but elevated temperature also decreased its survival. Elevated temperatures and CO2 further directly impeded the EPN infectivity potential, while lower moisture levels improved it through plant- and/or herbivore-mediated changes. In the RCP 8.5 scenario, temperature and CO2 showed interactive effects on EPN infectivity, which was overall decreased by 40%. We conclude that root pest problems may worsen with climate change due to increased herbivore performance and reduced top-down control by biological control agents.