Prioritizing plant defence over growth through WRKY regulation facilitates infestation by non-target herbivores

Plants generally respond to herbivore attack by increasing resistance and decreasing growth. This prioritization is achieved through the regulation of phytohormonal signaling networks. However, it remains unknown how this prioritization affects resistance against non-target herbivores. In this study, we identify WRKY70 as a specific herbivore-induced, mitogen-activated protein kinase-regulated rice transcription factor that physically interacts with W-box motifs and prioritizes defence over growth by positively regulating jasmonic acid (JA) and negatively regulating gibberellin (GA) biosynthesis upon attack by the chewing herbivore Chilo suppressalis. WRKY70-dependent JA biosynthesis is required for proteinase inhibitor activation and resistance against C. suppressalis. In contrast, WRKY70 induction increases plant susceptibility against the rice brown planthopper Nilaparvata lugens. Experiments with GA-deficient rice lines identify WRKY70-dependent GA signaling as the causal factor in N. lugens susceptibility. Our study shows that prioritizing defence over growth leads to a significant resistance trade-off with important implications for the evolution and agricultural exploitation of plant immunity.

Silencing OsHI-LOX makes rice more susceptible to chewing herbivores, but enhances resistance to a phloem feeder

The jasmonic acid (JA) pathway plays a central role in plant defense responses against insects. Some phloem-feeding insects also induce the salicylic acid (SA) pathway, thereby suppressing the plant’s JA response. These phenomena have been well studied in dicotyledonous plants, but little is known about them in monocotyledons. We cloned a chloroplast-localized type 2 13-lipoxygenase gene of rice, OsHI-LOX, whose transcripts were up-regulated in response to feeding by the rice striped stem borer (SSB) Chilo suppressalis and the rice brown planthopper (BPH) Niaparvata lugens, as well as by mechanical wounding and treatment with JA. Antisense expression of OsHI-LOX (as-lox) reduced SSB- or BPH-induced JA and trypsin protease inhibitor (TrypPI) levels, improved the larval performance of SBB as well as that of the rice leaf folder (LF) Cnaphalocrocis medinalis, and increased the damage caused by SSB and LF larvae. In contrast, BPH, a phloem-feeding herbivore, showed a preference for settling and ovipositing on WT plants, on which they consumed more and survived better than on as-lox plants. The enhanced resistance of as-lox plants to BPH infestation correlated with higher levels of BPH-induced H2O2 and SA, as well as with increased hypersensitive response-like cell death. These results imply that OsHI-LOX is involved in herbivore-induced JA biosynthesis, and plays contrasting roles in controlling rice resistance to chewing and phloem-feeding herbivores. The observation that suppression of JA activity results in increased resistance to an insect indicates that revision of the generalized plant defense models in monocotyledons is required, and may help develop novel strategies to protect rice against insect pests.

Canopy cover mediates interactions between a specialist caterpillar and seedlings of a neotropical tree

1 Light availability may be crucial for understanding dynamics of plant–herbivore interactions in temperate and tropical forest communities. This is because local light availability can influence both tree seedling tolerance and susceptibility to herbivory – yet how they mediate levels of insect herbivory that vary with the density of host population is virtually unknown. Here we tested predictions of three key, non-mutually exclusive hypotheses of plant–herbivore interactions: the Limiting Resource Model (LRM), the Plant Vigour Hypothesis (PVH), and the Janzen-Connell Mechanism (JCM). 2 In an Amazonian forest, we planted Swietenia macrophylla seedlings (c. 5 months old) into natural canopy gaps and the shaded understorey and simulated the damage patterns of the specialist herbivore moth, Steniscadia poliophaea, by clipping seedling leaves. Over the next 8 months, we monitored seedling performance in terms of growth and survivorship and also quantified herbivory to new young leaves on a seasonal basis. 3 In support of the LRM, severe leaf damage (≥ 50%) was lethal for Swietenia macrophylla seedlings in the understorey, but in gaps only reduced seedling growth. In support of the PVH, gap seedlings suffered greater post-simulated herbivory (up to 100% defoliation) by S. poliophaea caterpillars than their understorey counterparts. 4 Adding a novel dimension to the Janzen–Connell hypothesis, we found that early wet season herbivory of seedlings in gaps increased with conspecific adult density within a 125-m radius; whereas in the understorey only those seedlings within 50 m of a Swietenia tree were attacked by caterpillars. 5 Synthesis. These results suggest lepidopterans that need young leaves for food may forage more widely in forests to find seedlings in light-rich canopy gaps. Moths may achieve this successfully by being first attracted to gaps, and then searching within them for suitable hosts. A conceptual model, integrating conspecific adult tree density with light-driven changes in seedling tolerance/vigour and their susceptibility to herbivory and mortality, is presented. Spatial variation in the light available to tree seedlings often affects their tolerance and vigour, which may have important consequences for leaf-chewing insects and the scale of density-dependent herbivory in forests.

Sequestration of plant secondary metabolites by insect herbivores: molecular mechanisms and ecological consequences

Numerous insect herbivores can take up and store plant toxins as self-defense against their own natural enemies. Plant toxin sequestration is tightly linked with tolerance strategies that keep the toxins functional. Specific transporters have been identified that likely allow the herbivore to control the spatiotemporal dynamics of toxin accumulation. Certain herbivores furthermore possess specific enzymes to boost the bioactivity of the sequestered toxins. Ecologists have studied plant toxin sequestration for decades. The recently uncovered molecular mechanisms in combination with transient, non-transgenic systems to manipulate insect gene expression will help to understand the importance of toxin sequestration for food-web dynamics in nature.

A conserved pattern in plant-mediated interactions between herbivores

Plant‐mediated interactions between herbivores are important determinants of community structure and plant performance in natural and agricultural systems. Current research suggests that the outcome of the interactions is determined by herbivore and plant identity, which may result in stochastic patterns that impede adaptive evolution and agricultural exploitation. However, few studies have systemically investigated specificity versus general patterns in a given plant system by varying the identity of all involved players. We investigated the influence of herbivore identity and plant genotype on the interaction between leaf‐chewing and root‐feeding herbivores in maize using a partial factorial design. We assessed the influence of leaf induction by oral secretions of six different chewing herbivores on the response of nine different maize genotypes and three different root feeders. Contrary to our expectations, we found a highly conserved pattern across all three dimensions of specificity: The majority of leaf herbivores elicited a negative behavioral response from the different root feeders in the large majority of tested plant genotypes. No facilitation was observed in any of the treatment combinations. However, the oral secretions of one leaf feeder and the responses of two maize genotypes did not elicit a response from a root‐feeding herbivore. Together, these results suggest that plant‐mediated interactions in the investigated system follow a general pattern, but that a degree of specificity is nevertheless present. Our study shows that within a given plant species, plant‐mediated interactions between herbivores of the same feeding guild can be stable. This stability opens up the possibility of adaptations by associated organisms and suggests that plant‐mediated interactions may contribute more strongly to evolutionary dynamics in terrestrial (agro)ecosystems than previously assumed.

Mechanisms and evolution of plant resistance to aphids

Aphids are important herbivores of both wild and cultivated plants. Plants rely on unique mechanisms of recognition, signalling and defence to cope with the specialized mode of phloem feeding by aphids. Aspects of the molecular mechanisms underlying aphid-plant interactions are beginning to be understood. Recent advances include the identification of aphid salivary proteins involved in host plant manipulation, and plant receptors involved in aphid recognition. However, a complete picture of aphid-plant interactions requires consideration of the ecological outcome of these mechanisms in nature, and the evolutionary processes that shaped them. Here we identify general patterns of resistance, with a special focus on recognition, phytohormonal signalling, secondary metabolites and induction of plant resistance. We discuss how host specialization can enable aphids to co-opt both the phytohormonal responses and defensive compounds of plants for their own benefit at a local scale. In response, systemically induced resistance in plants is common and often involves targeted responses to specific aphid species or even genotypes. As co-evolutionary adaptation between plants and aphids is ongoing, the stealthy nature of aphid feeding makes both the mechanisms and outcomes of these interactions highly distinct from those of other herbivore-plant interactions. © 2016 Macmillan Publishers Limited.

Is fern endozoochory widespread among fern-eating herbivores?

Endozoochory is an important dispersal mechanism for seed plants and has recently been demonstrated to occur also in spore plants, such as ferns, which are commonly consumed by herbivores. However, it is not known whether fern species from particular habitats are differentially preferred by herbivores and whether their spores differ in their ability to survive the gut passage of herbivores. Such differences would suggest adaptation to endozoochorous dispersal, as it is known for seed plants. Moreover, it is unclear whether herbivore species differ in their efficiency to disperse fern spores. In a factorial experiment, we fed fertile leaflets of 13 fern species from different forest and open habitats to three polyphagous herbivore species and recorded the germination of spores from feces after 46 and 81 days. Fern spores germinated in 66 % of all samples after 46 days. At this stage, germination success differed among fern and herbivore species, but was independent of the ferns’ habitat. Interestingly, after 81 days fern spores germinated in 85 % of all samples and earlier significant differences in germination success among fern and herbivore species were not sustained. The overall high germination success and the absence of differences among fern species from different habitats together with the consistency across three tested herbivores strongly imply endozoochorous dispersal to be a taxonomically widespread phenomenon among fern-eating herbivores, which all might act as potential dispersal vectors. © 2015, Springer Science+Business Media Dordrecht.

Effects of genetic diversity of grass on insect species diversity at higher trophic levels are not due to cascading diversity effects

Genetic diversity in plant populations has been shown to affect the species diversity of insects. In grasses, infection with fungal endophytes can also have strong effects on insects, potentially modifying the effects of plant genetic diversity. We manipulated the genetic diversity and endophyte infection of a grass in a field experiment. We show that diversity of primary parasitoids (3rd trophic level) and, especially, secondary parasitoids (4th trophic level) increases with grass genetic diversity while there was no effect of endophyte infection. The increase in insect diversity appeared to be due to a complementarity effect rather than a sampling effect. The higher parasitoid diversity could not be explained by a cascading diversity effect because herbivore diversity was not affected and the same herbivore species were present in all treatments. The effects on the higher trophic levels must therefore be due to a direct response to plant traits or mediated by effects on traits at intermediate trophic levels.

A fungal endophyte helps plants to tolerate root herbivory through changes in gibberellin and jasmonate signaling

Plant–microbe mutualisms can improve plant defense, but the impact of root endophytes on below-ground herbivore interactions remains unknown. We investigated the effects of the root endophyte Piriformospora indica on interactions between rice (Oryza sativa) plants and its root herbivore rice water weevil (RWW; Lissorhoptrus oryzophilus), and how plant jasmonic acid (JA) and GA regulate this tripartite interaction. Glasshouse experiments with wild-type rice and coi1-18 and Eui1-OX mutants combined with nutrient, jasmonate and gene expression analyses were used to test: whether RWW adult herbivory above ground influences subsequent damage caused by larval herbivory below ground; whether P. indica protects plants against RWW; and whether GA and JA signaling mediate these interactions. The endophyte induced plant tolerance to root herbivory. RWW adults and larvae acted synergistically via JA signaling to reduce root growth, while endophyte-elicited GA biosynthesis suppressed the herbivore-induced JA in roots and recovered plant growth. Our study shows for the first time the impact of a root endophyte on plant defense against below-ground herbivores, adds to growing evidence that induced tolerance may be an important root defense, and implicates GA as a signal component of inducible plant tolerance against biotic stress.

Different-sized grazers have distinctive effects on plant functional composition of an African savannah

Grazing ungulates play a key role in many ecosystems worldwide and can form diverse assemblages, such as in African savannahs. In many of these ecosystems, present-day ungulate communities are impoverished subsets of once diverse assemblages. While we know that excluding all ungulates from grasslands can exert major effects on both the structure and composition of the vegetation, how different individual ungulate species may have contrasting effects on grassland communities remains poorly understood. Here, we performed a long-term ‘Russian doll’ grazing exclosure experiment in an African savannah to test for the effects of different size classes of grazers on grassland structure and composition. At five sites, grazer species of decreasing size class (ranging from white rhino to scrub hare) were excluded using four fence types, to experimentally create different realized grazer assemblages. The vegetation structure and the grass functional community composition were characterized in 6 different years over a 10-year period. Additionally, animal footprints were counted to quantify the abundance of different ungulate species in each treatment. We found that while vegetation height was mostly driven by total grazing pressure of all species together, ungulate community composition best explained the functional community composition of grasses. In the short term, smaller ungulate species (‘mesoherbivores’) had strongest effects on vegetation composition, by shifting communities towards dominance by species with low specific leaf area and low nutritional value. In the long term, large grazers had stronger but similar effects on the functional composition of the system. Surprisingly, the largest ‘mega-herbivore’, the white rhinoceros, did not have strong effects on the vegetation structure or composition. Synthesis. Our results support the idea that different size classes of grazers have varying effects on the functional composition of grassland plant communities. Therefore, the worldwide decline in the diversity of ungulate species is expected to have (had) major impacts on community composition and functioning of grassland ecosystems, even if total grazing pressure has remained constant, for example, due to replacement by livestock.

Criminal Solicitation, Entrapment, and the Enforcement of Law

This paper examines the optimal use of criminal solicitation as a law enforcement strategy. The benefits are greater deterrence of crime (due to the greater likelihood of apprehension), and the savings in social harm as some offenders are diverted away from committing actual crimes through solicitation. The costs are the expense of hiring undercover cops and the greater likelihood of punishment. The optimal use of solicitation balances these factors. The paper also examines the justification for the entrapment defense, which exonerates those caught in a criminal solicitation but who otherwise had no predisposition to commit a crime.

Criminal Solicitation, Entrapment, and the Enforcement of Law

This paper examines the optimal use of criminal solicitation as a law enforcement strategy. The benefits are greater deterrence of crime (due to the greater likelihood of apprehension), and the savings in social harm and apprehension costs as some offenders are diverted away from committing actual crimes through solicitation. The costs are the expense of hiring undercover cops and the greater likelihood of punishment. The optimal use of solicitation balances these factors. The paper also examines the justification for, and impact of, the entrapment defense, which exonerates those caught in a solicitation but otherwise not predisposed to commit a crime.

Punishing the Innocent along with the Guilty: The Economics of Individual versus Group Punishment

Standard models of law enforcement involve the apprehension and punishment of a single suspect, but in many contexts, punishment is actually imposed on an entire group known to contain the offender. The advantages of .group punishment. are that the offender is punished with certainty and detection costs are saved. The disadvantage is that innocent individuals are punished. We compare individual and group punishment when social welfare depends on fairness, and when it depends on deterrence. We show that group punishment may dominate in the former case if the detection technology is ineffective but never in the latter case. We discuss our results in the context of several examples.

The Social versus Private Incentive to Sue

The private value of lawsuits is based on plaintiffs' expected recovery at trial compared to their filing costs, whereas the social value consists of the incentives suits create for injurers to invest in accident avoidance. Generally, there is no relationship between these two values: there may be either too many or too few suits from a social perspective. Thus, there is scope for corrective measures, although there is no simple policy. Extending the model to consider a negligence rule rather than strict liability, and to allow for pretrial settlements, leads to some modified conclusions but does not alter the basic insights.

A Note on the Social versus Private Value of Suits when Care is Bilateral

This paper re-examines the social versus private value of lawsuits when both injurers and victims can take care. The basic conclusions of that literature remain valid in this context: the private and social values generally differ, and there is no necessary relationship between them, meaning that there may be either too many or too few suits. Introducing the possibility of victim care does, however, alter the calculation of the deterrent effect of lawsuits. In particular, because allowing suits tends to reduce the incentives for victims to invest in precaution, the social value of prohibiting suits increases in direct relation to the productivity of victim care in lowering accident risk.