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Herbivore-induced plant volatiles prime plant defenses and resistance, but how they are integrated into early defense signaling and whether a causal relationship exists between volatile defense priming and herbivore resistance is unclear. Here, we investigated the impact of indole, a common herbivore-induced plant volatile and modulator of many physiological processes in plants, bacteria, and animals, on early defense signaling and herbivore resistance in rice (Oryza sativa). Rice plants infested by fall armyworm (Spodoptera frugiperda) caterpillars release indole at a rate of up to 25 ng*h−1. Exposure to equal doses of exogenous indole enhances rice resistance to S. frugiperda. Screening of early signaling components revealed that indole pre-exposure directly enhances the expression of the leucine-rich repeat-receptor-like kinase OsLRR-RLK1. Pre-exposure to indole followed by simulated herbivory increases (i.e. primes) the transcription, accumulation, and activation of the mitogen-activated protein kinase OsMPK3 and the expression of the downstream WRKY transcription factor gene OsWRKY70 as well as several jasmonate biosynthesis genes, resulting in higher jasmonic acid (JA) accumulation. Analysis of transgenic plants defective in early signaling showed that OsMPK3 is required and that OsMPK6 and OsWRKY70 contribute to indole-mediated defense priming of JA-dependent herbivore resistance. Therefore, herbivore-induced plant volatiles increase plant resistance to herbivores by positively regulating early defense signaling components.

In high-risk environments with frequent predator encounters, efficient antipredator behavior is key to survival. Parental effects are a powerful mechanism to prepare offspring for coping with such environments, yet clear evidence for adaptive parental effects on offspring antipredator behaviors is missing. Rapid escape reflexes, or “C-start reflexes,” are a key adaptation in fish and amphibians to escape predator strikes. We hypothesized that mothers living in high-risk environments might induce faster C-start reflexes in offspring by modifying egg composition. Here, we show that offspring of the cichlid fish Neolamprologus pulcher developed faster C-start reflexes and were more risk averse if their parents had been exposed to cues of their most dangerous natural predator during egg production. This effect was mediated by differences in egg composition. Eggs of predator-exposed mothers were heavier with higher net protein content, and the resulting offspring were heavier and had lower igf-1 gene expression than control offspring shortly after hatching. Thus, changes in egg composition can relay multiple putative pathways by which mothers can influence adaptive antipredator behaviors such as faster escape reflexes.

By changing soil properties, plants can modify their growth environment. Although the soil microbiota is known to play a key role in the resulting plant-soil feedbacks, the proximal mechanisms underlying this phenomenon remain unknown. We found that benzoxazinoids, a class of defensive secondary metabolites that are released by roots of cereals such as wheat and maize, alter root-associated fungal and bacterial communities, decrease plant growth, increase jasmonate signaling and plant defenses, and suppress herbivore performance in the next plant generation. Complementation experiments demonstrate that the benzoxazinoid breakdown product 6-methoxy-benzoxazolin-2-one (MBOA), which accumulates in the soil during the conditioning phase, is both sufficient and necessary to trigger the observed phenotypic changes. Sterilization, fungal and bacterial profiling and complementation experiments reveal that MBOA acts indirectly by altering root-associated microbiota. Our results reveal a mechanism by which plants determine the composition of rhizosphere microbiota, plant performance and plant-herbivore interactions of the next generation. Plants can modify soil microbiota through root exudation, but how this process influences plant health in turn is often unclear. Here, Hu et al. show that maize benzoxazinoids released into the soil modify root-associated microbiota and thereby increase leaf defenses of the next plant generation.

Plants are constantly exposed to a variety of environmental stresses, including herbivory. How plants perceive herbivores on a molecular level is poorly understood. Leucine-rich repeat receptor-like kinases (LRR-RLKs), the largest subfamily of RLKs, are essential for plants to detect external stress signals, and may therefore also be involved in herbivore perception. Here, we employed RNA interference silencing, phytohormone profiling and complementation, as well as herbivore resistance assays, to investigate the requirement of an LRR-RLK for the initiation of rice (Oryza sativa) defenses against the chewing herbivore striped stem borer (SSB) Chilo suppressalis. We discovered a plasma membrane-localized LRR-RLK, OsLRR-RLK1, whose transcription is strongly up-regulated by SSB attack and treatment with oral secretions of Spodoptera frugiperda. OsLRR-RLK1 acts upstream of mitogen-activated protein kinase (MPK) cascades, and positively regulates defense-related MPKs and WRKY transcription factors. Moreover, OsLRR-RLK1 is a positive regulator of SSB-elicited, but not wound-elicited, levels of jasmonic acid and ethylene, trypsin protease inhibitor activity and plant resistance towards SSB. OsLRR-RLK1 therefore plays an important role in herbivory-induced defenses of rice. Given the well-documented role of LRR-RLKs in the perception of stress-related molecules, we speculate that OsLRR-RLK1 may be involved in the perception of herbivory-associated molecular patterns.

413 I. 413 II. 414 III. 414 IV. 415 V. 416 VI. 417 VII. 417 417 References 417 SUMMARY: The distinctive ecology of root herbivores, the complexity and diversity of root–microbe interactions, and the physical nature of the soil matrix mean that plant responses to root herbivory extrapolate poorly from our understanding of responses to aboveground herbivores. For example, root attack induces different changes in phytohormones to those in damaged leaves, including a lower but more potent burst of jasmonates in several plant species. Root secondary metabolite responses also differ markedly, although patterns between roots and shoots are harder to discern. Root defences must therefore be investigated in their own ecophysiological and evolutionary context, specifically one which incorporates root microbial symbionts and antagonists, if we are to better understand the battle between plants and their hidden herbivores.

Plants respond to herbivory by reconfiguring hormonal networks, increasing secondary metabolite production and decreasing growth. Furthermore, some plants display a decrease in leaf energy reserves in the form of soluble sugars and starch, leading to the hypothesis that herbivory-induced secondary metabolite production and growth reduction may be linked through a carbohydrate-based resource trade-off. In order to test the above hypothesis, we measured leaf carbohydrates and plant growth in seven genetically engineered Nicotiana attenuata genotypes that are deficient in one or several major herbivore-induced, jasmonate-dependent defensive secondary metabolites and proteins. Furthermore, we manipulated gibberellin and jasmonate signaling, and quantified the impact of these phytohormones on secondary metabolite production, sugar accumulation and growth. Simulated herbivore attack by Manduca sexta specifically reduced leaf sugar concentrations and growth in a jasmonate-dependent manner. These effects were similar or even stronger in defenseless genotypes with intact jasmonate signaling. Gibberellin complementation rescued carbohydrate accumulation and growth in induced plants without impairing the induction of defensive secondary metabolites. These results are consistent with a hormonal antagonism model rather than a resource–cost model to explain the negative relationship between herbivory-induced defenses, leaf energy reserves and growth.

Herbivore-induced volatile organic compounds prime non-attacked plant tissues to respond more strongly to subsequent attacks. However, the key volatiles that trigger this primed state remain largely unidentified. In maize, the release of the aromatic compound indole is herbivore-specific and occurs earlier than other induced responses. We therefore hypothesized that indole may be involved in airborne priming. Using indole-deficient mutants and synthetic indole dispensers, we show that herbivore-induced indole enhances the induction of defensive volatiles in neighbouring maize plants in a species-specific manner. Furthermore, the release of indole is essential for priming of mono- and homoterpenes in systemic leaves of attacked plants. Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming. These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks. Herbivore attack of plant tissue primes non-attacked tissue to respond more strongly to subsequent attacks. Here, Erb et al . identify indole as an airborne priming signal that enhances herbivore-induced defensive-volatile and stress-hormone production in systemic tissues and neighbouring plants.

Root herbivores are important ecosystem drivers and agricultural pests, and, possibly as a consequence, plants protect their roots using a variety of defensive strategies. One aspect that distinguishes belowground from aboveground plant–insect interactions is that roots are constantly exposed to a set of soil-specific abiotic factors. These factors can profoundly influence root resistance, and, consequently, the outcome of the interaction with belowground feeders. In this review, we synthesize the current literature on the impact of soil moisture, nutrients, and texture on root–herbivore interactions. We show that soil abiotic factors influence the interaction by modulating herbivore abundance and behaviour, root growth and resistance, beneficial microorganisms, as well as natural enemies of the herbivores. We suggest that abiotic heterogeneity may explain the high variability that is often encountered in root–herbivore systems. We also propose that under abiotic stress, the relative fitness value of the roots and the potential negative impact of herbivory increases, which may lead to a higher defensive investment and an increased recruitment of beneficial microorganisms by the plant. At the same time, both root-feeding herbivores and natural enemies are likely to decrease in abundance under extreme environmental conditions, leading to a context- and species-specific impact on plant fitness. Only by using tightly controlled experiments that include soil abiotic heterogeneity will it be possible to understand the impact of root feeders on an ecosystem scale and to develop predictive models for pest occurrence and impact.

Plants encounter natural antagonist threats of varying intensity and respond by activating multiple defense traits. Due to the fitness costs associated with producing defense traits, plants are expected to activate less costly traits first, reserving more costly defenses for potentially more severe damage (“cheaper first hypothesis”), but evidence to date is scarce. Here, we tested this hypothesis by measuring six putative defense traits in the annual plant Ambrosia artemisiifolia . We found that all traits were effective against insect herbivores, but production of three of them more strongly reduced plant growth, suggesting higher growth costs. When plants were attacked by insect herbivores, less costly traits were induced first, even at the lowest levels of damage, while more costly traits were activated only after higher damage thresholds. This cost-dependent sequential pattern was consistently observed in plants when challenged by 12 different herbivore species from three insect orders. These findings demonstrate that plants can employ the “cheaper first” sequential induction defense strategy, potentially allowing them to reduce defense costs and maximize fitness. Our study provides new insights into how plants fine-tune their defense responses under variable antagonistic pressures.

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. Many different animals feed on plants, including almost half of all known insect species. Some herbivores—like caterpillars for example—feed by chewing. Others, such as aphids and planthoppers, use syringe-like mouthparts to pierce plants and then feed on the fluids within. To minimize the damage caused by these herbivores, plants activate specific defenses upon attack, including proteins that can inhibit the insect's digestive enzymes. The inhibitors are effective against chewing herbivores but seem to have little or no effect on some insects that feed by the ‘pierce-and-suck’ method. Investing in defense requires energy, and so plants attacked by herbivores actively slow their growth to meet this demand. Plants achieve this trade-off by changing the levels of different plant hormones. These hormones can control the expression of thousands of genes and have widespread effects throughout the plant. However, little is known about how prioritizing defense overgrowth in response to an attack by one herbivore affects the plant's ability to defend itself against other herbivores. Transcription factors are proteins that control which genes inside a cell are active or inactive. Li et al. searched for a transcription factor in rice plants that was specifically triggered in response to an attack by the caterpillars of a moth called the rice striped stem borer. This search identified a protein called WRKY70 as a transcription factor that prioritizes defense overgrowth. WRKY70 achieves this by increasing the levels of a defensive plant hormone (called jasmonic acid) while reducing the levels of a growth hormone (called gibberellin). Further experiments show that the increase in jasmonic acid production is required to activate the enzyme inhibitors and for resistance against these caterpillars. Li et al. then found that increased WRKY70 activity makes rice plants more susceptible to attack by a second herbivore, a piercing-sucking insect called the rice brown planthopper. Further experiments revealed that this is due to the reduced levels of gibberillin. These findings show that while prioritizing defense overgrowth is effective against some insect herbivores, it comes with a cost as it makes the plants more susceptible to attack by other herbivores. This trade-off has important implications for both the evolution of plant immunity, and efforts to exploit plant immunity to help protect crops from herbivore attack.