Ricca's factors as mobile proteinaceous effectors of electrical signaling.

Leaf-feeding insects trigger high-amplitude, defense-inducing electrical signals called slow wave potentials (SWPs). These signals are thought to be triggered by the long-distance transport of low molecular mass elicitors termed Ricca's factors. We sought mediators of leaf-to-leaf electrical signaling in Arabidopsis thaliana and identified them as ß-THIOGLUCOSIDE GLUCOHYDROLASE 1 and 2 (TGG1 and TGG2). SWP propagation from insect feeding sites was strongly attenuated in tgg1 tgg2 mutants and wound-response cytosolic Ca2+ increases were reduced in these plants. Recombinant TGG1 fed into the xylem elicited wild-type-like membrane depolarization and Ca2+ transients. Moreover, TGGs catalyze the deglucosidation of glucosinolates. Metabolite profiling revealed rapid wound-induced breakdown of aliphatic glucosinolates in primary veins. Using in vivo chemical trapping, we found evidence for roles of short-lived aglycone intermediates generated by glucosinolate hydrolysis in SWP membrane depolarization. Our findings reveal a mechanism whereby organ-to-organ protein transport plays a major role in electrical signaling.

Rethinking livestock encroachment at a protected area boundary.

The presence of livestock inside protected areas, or "livestock encroachment," is a global conservation concern because livestock is broadly thought to negatively affect wildlife. The Maasai Mara National Reserve (MMNR), Kenya, exemplifies this tension as livestock is believed to have resulted in the declining wildlife populations, contributing to the strict and sometimes violent exclusion measures targeting Maasai pastoralists. However, research embedded in the real-world setting that draws insights from the social-ecological contexts is lacking. In this study, we conducted 19 mo of ecological monitoring covering 60 sites in MMNR and found that cattle presence inside the reserve did not significantly impact most co-occurring wild herbivores at the current intensity. Using the Hierarchical Modeling of Species Communities and Gaussian copula graphic models, we showed that cattle had no direct associations-neither negative nor positive-with nearly all wild herbivores despite frequently sharing the same space. Moreover, we did not detect resource degradation correlated with cattle presence near the MMNR boundary. Given the colonial legacy and land use history of Mara, entering MMNR becomes the only viable option for many herders. These results corroborate the emerging perspective that the ecological impacts of extensively herded livestock on wildlife might be more nuanced than previously thought. To effectively balance the needs of people, livestock, and wildlife, the current rigid livestock exclusion measures need to be reassessed to holistically consider herbivore ecology, local land use history, and modern politics of protected area management.

Fossil leaves reveal drivers of herbivore functional diversity during the Cenozoic.

Herbivorous arthropods are the most diverse group of multicellular organisms on Earth. The most discussed drivers of their inordinate taxonomic and functional diversity are high niche availability associated with the diversity of host plants and dense niche packing due to host partitioning among herbivores. However, the relative contributions of these two factors to dynamics in the diversity of herbivores throughout Earth's history remain unresolved. Using fossil data on herbivore-induced leaf damage from across the Cenozoic, we infer quantitative bipartite interaction networks between plants and functional feeding types of herbivores. We fit a general model of diversity to these interaction networks and discover that host partitioning among functional groups of herbivores contributed twice as much to herbivore functional diversity as host diversity. These findings indicate that niche packing primarily shaped the dynamics in the functional diversity of herbivores during the past 66 my. Our study highlights how the fossil record can be used to test fundamental theories of biodiversity and represents a benchmark for assessing the drivers of herbivore functional diversity in modern ecosystems.

A conserved protein family in mirid bug Riptortus pedestris plays dual roles in regulating plant immunity.

The mirid bug (Riptortus pedestris), a major soybean pest, migrates into soybean fields during the pod filling stage and causes staygreen syndrome, which leads to substantial yield losses. The mechanism by which R. pedestris elicits soybean (Glycine max) defenses and counter-defenses remains largely unexplored. In this study, we characterized a protein family from R. pedestris, designated Riptortus pedestris HAMP 1 (RPH1) and its putative paralogs (RPH1L1, 2, 3, 4, and 5), whose members exhibit dual roles in triggering and inhibiting plant immunity. RPH1 and RPH1L1 function as herbivore-associated molecular patterns (HAMPs), activating pattern-triggered immunity (PTI) in tobacco (Nicotiana benthamiana) and G. max. Furthermore, RPH1 stimulates jasmonic acid and ethylene biosynthesis in G. max, thereby enhancing its resistance to R. pedestris feeding. Additionally, RPH1 homologs are universally conserved across various herbivorous species, with many homologs also acting as HAMPs that trigger plant immunity. Interestingly, the remaining RPH1 putative paralogs (RPH1L2-5) serve as effectors that counteract RPH1-induced PTI, likely by disrupting the extracellular perception of RPH1. This research uncovers a HAMP whose homologs are conserved in both chewing and piercing-sucking insects. Moreover, it unveils an extracellular evasion mechanism utilized by herbivores to circumvent plant immunity using functionally differentiated paralogs.

Sublethal effects of parasitism on ruminants can have cascading consequences for ecosystems.

Parasitic infections are common, but how they shape ecosystem-level processes is understudied. Using a mathematical model and meta-analysis, we explored the potential for helminth parasites to trigger trophic cascades through lethal and sublethal effects imposed on herbivorous ruminant hosts after infection. First, using the model, we linked negative effects of parasitic infection on host survival, fecundity, and feeding rate to host and producer biomass. Our model, parameterized with data from a well-documented producer­caribou­helminth system, reveals that even moderate impacts of parasites on host survival, fecundity, or feeding rate can have cascading effects on ruminant host and producer biomass. Second, using meta-analysis, we investigated the links between helminth infections and traits of free-living ruminant hosts in nature. We found that helminth infections tend to exert negative but sublethal effects on ruminant hosts. Specifically, infection significantly reduces host feeding rates, body mass, and body condition but has weak and highly variable effects on survival and fecundity. Together, these findings suggest that while helminth parasites can trigger trophic cascades through multiple mechanisms, overlooked sublethal effects on nonreproductive traits likely dominate their impacts on ecosystems. In particular, by reducing ruminant herbivory, pervasive helminth infections may contribute to a greener world.

Pest Status, Bio-Ecology, and Area-Wide Management of Mirids in East Asia.

Mirids (Hemiptera: Heteroptera: Miridae) feed upon a wide variety of cultivated and wild plants and can be economically important crop pests. They have traditionally been perceived as innocuous herbivores in East Asia; however, population levels of various mirid species have dramatically increased over the past decades. High-profile pests such as Apolygus spp., Adelphocoris spp., and Lygus spp. are now widely distributed across the region, and their infestation pressure is associated with climate, agroecological conditions, and farming practices. This review outlines how an in-depth understanding of pest biology, a systems-level characterization of pest ecology, and a comprehensive evaluation of integrated pest management tactics have enabled sustainable management of mirids across crop boundaries and harvest cycles. This work underscores how more holistic, integrative research approaches can accelerate the implementation of area-wide management of generalist pests, effectively prevent pest population build-up and yield impact, and shrink the environmental footprint of agriculture. In addition to highlighting the merits of interdisciplinary systems approaches, we discuss prospects and challenges for the sustainable management of polyphagous mirid pests in landscape matrices.

Grazing herbivores reduce herbaceous biomass and fire activity across African savannas.

Fire and herbivory interact to alter ecosystems and carbon cycling. In savannas, herbivores can reduce fire activity by removing grass biomass, but the size of these effects and what regulates them remain uncertain. To examine grazing effects on fuels and fire regimes across African savannas, we combined data from herbivore exclosure experiments with remotely sensed data on fire activity and herbivore density. We show that, broadly across African savannas, grazing herbivores substantially reduce both herbaceous biomass and fire activity. The size of these effects was strongly associated with grazing herbivore densities, and surprisingly, was mostly consistent across different environments. A one-zebra increase in herbivore biomass density (~100 kg/km2 of metabolic biomass) resulted in a ~53 kg/ha reduction in standing herbaceous biomass and a ~0.43 percentage point reduction in burned area. Our results indicate that fire models can be improved by incorporating grazing effects on grass biomass.

The biogeochemical boomerang: Site fidelity creates nutritional hotspots that may promote recurrent calving site reuse.

Animals interact with nutrient cycles by consuming and depositing nutrients, interactions studied separately in nutritional ecology and zoogeochemistry. Recent theoretical work bridges these disciplines, highlighting that animal-driven nutrient recycling could be crucial in helping animals meet their nutritional needs. When animals exhibit site fidelity, they consistently deposit nutrients, potentially improving vegetation quality. We investigated this potential feedback by analysing changes in forage nitrogen stocks following simulated caribou calving. We found that forage nitrogen stocks increased after 2 weeks and remained elevated after 1 year, a change due to increased forage quality, not quantity. We also developed a nutrient budget within calving grounds, demonstrating that natal fluid and calf carcasses contribute substantial nitrogen subsidies. We, thus, highlight a positive zoogeochemical feedback whereby nutrients deposited during calving become bioavailable during lactation and provide evidence that site fidelity creates a biogeochemical boomerang in which animals deposit nutrients that can be reused later.

Mean reef fish body size decreases towards warmer waters.

Aquatic ectotherms often attain smaller body sizes at higher temperatures. By analysing ~15,000 coastal-reef fish surveys across a 15°C spatial sea surface temperature (SST) gradient, we found that the mean length of fish in communities decreased by ~5% for each 1°C temperature increase across space, or 50% decrease in mean length from 14 to 29°C mean annual SST. Community mean body size change was driven by differential temperature responses within trophic groups and temperature-driven change in their relative abundance. Herbivores, invertivores and planktivores became smaller on average in warmer temperatures, but no trend was found in piscivores. Nearly 25% of the temperature-related community mean size trend was attributable to trophic composition at the warmest sites, but at colder temperatures, this was <1% due to trophic groups being similarly sized. Our findings suggest that small changes in temperature are associated with large changes in fish community composition and body sizes, with important ecological implications.

Evolutionary Systems Biology Identifies Genetic Trade-offs In Rice Defense Against Above- and Belowground Attackers.

Like other plants, wild and domesticated rice species (Oryza nivara, O. rufipogon, and O. sativa) evolve in environments with various biotic and abiotic stresses that fluctuate in intensity through space and time. Microbial pathogens and invertebrate herbivores such as plant-parasitic nematodes and caterpillars show geographical and temporal variation in activity patterns and may respond differently to certain plant defensive mechanisms. As such, plant interactions with multiple community members may result in conflicting selection pressures on genetic polymorphisms. Here, through assays with different above- and belowground herbivores, the fall armyworm (Spodoptera frugiperda) and the southern root-knot nematode (Meloidogyne incognita), respectively, and comparison with rice responses to microbial pathogens, we identify potential genetic trade-offs at the KSL8 and MG1 loci on chromosome 11. KSL8 encodes the first committed step towards biosynthesis of either stemarane- or stemodane-type diterpenoids through the japonica (KSL8-jap) or indica (KSL8-ind) allele. Knocking out KSL8-jap and CPS4, encoding an enzyme that acts upstream in diterpenoid synthesis, in japonica rice cultivars increased resistance to S. frugiperda and decreased resistance to M. incognita. Furthermore, MG1 resides in a haplotype that provided resistance to M. incognita, while alternative haplotypes are involved in mediating resistance to the rice blast fungus Magnaporthe oryzae and other pests and pathogens. Finally, KSL8 and MG1 alleles are located within trans-species haplotypes and may be evolving under long-term balancing selection. Our data are consistent with a hypothesis that polymorphisms at KSL8 and MG1 may be maintained through complex and diffuse community interactions.

Limonene enhances rice plant resistance to a piercing-sucking herbivore and rice pathogens.

Terpene synthases (TPSs) are key enzymes in terpenoids synthesis of plants and play crucial roles in regulating plant defence against pests and diseases. Here, we report the functional characterization of OsTPS19 and OsTPS20, which were upregulated by the attack of brown planthopper (BPH). BPH female adults performed concentration-dependent behavioural responses to (S)-limonene showing preference behaviour at low concentrations and avoidance behaviour at high concentrations. Overexpression lines of OsTPS19 and OsTPS20, which emitted higher amounts of the monoterpene (S)-limonene, decreased the hatching rate of BPH eggs, reduced the lesion length of sheath blight caused by Rhizoctonia solani and bacterial blight caused by Xanthomonas oryzae. While knockout lines of OsTPS19 and OsTPS20, which emitted lower amounts of (S)-limonene, were more susceptible to these pathogens. Overexpression of OsTPS19 and OsTPS20 in rice plants had adverse effects on the incidence of BPH, rice blast, and sheath blight in the field and had no significant impacts on rice yield traits. OsTPS19 and OsTPS20 were found to be involved in fine-tuning the emission of (S)-limonene in rice plants and play an important role in defence against both BPH and rice pathogens.

How does plant chemodiversity evolve? Testing five hypotheses in one population genetic model.

Plant chemodiversity, the diversity of plant-specialized metabolites, is an important dimension of biodiversity. However, there are so far few mathematical models to test verbal hypotheses on how chemodiversity evolved. Here, we develop such a model to test predictions of five hypotheses: the 'fluctuating selection hypothesis', the 'dominance reversal hypothesis', the interaction diversity hypothesis, the synergy hypothesis, and the screening hypothesis. We build a population genetic model of a plant population attacked by herbivore species whose occurrence fluctuates over time. We study the model using mathematical analysis and individual-based simulations. As predicted by the 'dominance reversal hypothesis', chemodiversity can be maintained if alleles conferring a defense metabolite are dominant with respect to the benefits, but recessive with respect to costs. However, even smaller changes in dominance can maintain polymorphism. Moreover, our results underpin and elaborate predictions of the synergy and interaction diversity hypotheses, and, to the extent that our model can address it, the screening hypotheses. By contrast, we found only partial support for the 'fluctuating selection hypothesis'. In summary, we have developed a flexible model and tested various verbal models for the evolution of chemodiversity. Next, more mechanistic models are needed that explicitly consider the organization of metabolic pathways.

Legacy effects of premature defoliation in response to an extreme drought event modulate phytochemical profiles with subtle consequences for leaf herbivory in European beech.

Extreme droughts can have long-lasting effects on forest community dynamics and species interactions. Yet, our understanding of how drought legacy modulates ecological relationships is just unfolding. We tested the hypothesis that leaf chemistry and herbivory show long-term responses to premature defoliation caused by an extreme drought event in European beech (Fagus sylvatica L.). For two consecutive years after the extreme European summer drought in 2018, we collected leaves from the upper and lower canopy of adjacently growing drought-stressed and unstressed trees. Leaf chemistry was analyzed and leaf damage by different herbivore-feeding guilds was quantified. We found that drought had lasting impacts on leaf nutrients and on specialized metabolomic profiles. However, drought did not affect the primary metabolome. Drought-related phytochemical changes affected damage of leaf-chewing herbivores whereas damage caused by other herbivore-feeding guilds was largely unaffected. Drought legacy effects on phytochemistry and herbivory were often weaker than between-year or between-canopy strata variability. Our findings suggest that a single extreme drought event bears the potential to long-lastingly affect tree-herbivore interactions. Drought legacy effects likely become more important in modulating tree-herbivore interactions since drought frequency and severity are projected to globally increase in the coming decades.

Belowground insect herbivory induces systemic volatile emissions that strengthen neighbouring plant resistance aboveground.

Plants transmit ecologically relevant messages to neighbouring plants through chemical cues. For instance, insect herbivory triggers the production of herbivore-induced plant volatiles (HIPVs), which can enhance neighbouring plant defences. HIPVs are emitted from directly damaged plant tissues and from systemic, nondamaged tissues. Although volatile-mediated interplant interactions have been observed both above- and belowground, it remains unknown whether belowground herbivory induces systemic HIPVs aboveground that influence neighbouring plants. To explore how belowground herbivory affects interplant interactions aboveground, we characterised systemic HIPVs from squash induced by belowground striped cucumber beetle (Acalymma vittatum) larval herbivory. We exposed squash 'receiver plants' to systemic HIPVs or volatiles from nondamaged plants. We then measured herbivore resistance by challenging 'receiver plants' with aboveground-feeding herbivores: adult beetles (A. vittatum) or squash bugs (Anasa tristis). We discovered belowground-damaged plants emitted more (E)-ß-ocimene, a key volatile from the systemic HIPV blend, than nondamaged controls, and that exposure to systemic HIPVs enhanced neighbouring plant resistance to aboveground squash bugs, but not adult beetles. Further investigations into the mechanism of interplant interaction revealed ß-ocimene alone can elicit plant resistance against squash bugs. Overall, our findings reveal a novel form of volatile-mediated interactions between plants spanning across aboveground-belowground plant systems.

UGT89AC1-mediated quercetin glucosylation is induced upon herbivore damage and enhances Camellia sinensis resistance to insect feeding.

Quercetin is a key flavonol in tea plants (Camellia sinensis (L.) O. Kuntze) with various health benefits, and it often occurs in the form of glucosides. The roles of quercetin and its glucosylated forms in plant defense are generally not well-studied, and remain unknown in the defense of tea. Here, we found higher contents of quercetin glucosides and a decline of the aglucone upon Ectropis grisescens (E. grisescens) infestation of tea. Nine UGTs were strongly induced, among which UGT89AC1 exhibited the highest activity toward quercetin in vitro and in vivo. The mass of E. grisescens larvae that fed on plants with repressed UGT89AC1 or varieties with lower levels of UGT89AC1 was significantly lower than that of larvae fed on controls. Artificial diet supplemented with quercetin glucoside also reduced the larval growth rate, whereas artificial diet supplemented with free quercetin had no significant effect on larval growth. UGT89AC1 was located in both the cytoplasm and nucleus, and its expression was modulated by JA, JA-ILE, and MeJA. These findings demonstrate that quercetin glucosylation serves a defensive role in tea against herbivory. Our results also provide novel insights into the ecological relevance of flavonoid glycosides under biotic stress in plants.

The jasmonate pathway and water loss in rice leaves induced by a stem-borer inhibit leaf-feeder growth.

Plant-mediated interactions between herbivores play an important role in regulating the composition of herbivore community. The fall armyworm (FAW), Spodoptera frugiperda, which has become one of the most serious pests on corn in China since it invaded in 2018, has been found feeding rice in the field. However, how FAW interacts with native rice insect pests remains largely unknown. Here, we investigated the interaction between FAW and a resident herbivore, striped stem borer (SSB, Chilo suppressalis) on rice. The infestation of rice leaf sheaths (LSs) by SSB larvae systemically enhanced the level of jasmonic acid (JA), abscisic acid (ABA), and trypsin proteinase inhibitors (TPIs), reduced relative water content (RWC) in leaf blades (LBs), and suppressed the growth of FAW larvae. In contrast, because FAW larvae infested LBs and did not affect defence responses in LSs, they did not influence the performance of SSB larvae. Using different mutants, together with bioassays and chemical analysis, we revealed that SSB-induced suppression of FAW larvae growth depended on both the SSB-activated JA pathway and RWC in LBs, whereas the ABA pathway activated by SSB larvae promoted the growth of FAW larvae by impeding water loss. These results provide new insights into mechanisms underlying plant-mediated interactions between herbivores.

Entomopathogenic Nematodes-Killed Insect Cadavers in the Rhizosphere Activate Plant Direct and Indirect Defences Aboveground.

Plants can perceive and respond to external stimuli by activating both direct and indirect defences against herbivores. Soil-dwelling entomopathogenic nematodes (EPNs), natural enemies of root-feeding herbivores, carry symbiotic bacteria that grow and reproduce once inside arthropod hosts. We hypothesized that the metabolites produced by EPN-infected insect cadavers could be perceived by plants, thereby activating plant defences systemically. We tested this hypothesis by adding three EPN-infected Galleria mellonella cadavers to maize plants and testing plant responses against a major maize pest (Spodoptera frugiperda) and one of its parasitoids (Trichogramma dendrolimi). We found that S. frugiperda females deposited fewer, and caterpillars fed less on maize plants growing near EPN-infected cadavers than on control plants. Accordingly, EPN-infected cadavers triggered the systemic accumulation of defence hormones (SA), genes (PR1), and enzymes (SOD, POD, and CAT) in maize leaves. Furthermore, four volatile organic compounds produced by plants exposed to EPN-infected cadavers deterred S. frugiperda caterpillars and female adults. However, these compounds were more attractive to T. dendrolimi parasitoids. Our study enhances the understanding of the intricate relationships within the above- and belowground ecosystems and provides crucial insights for advancing sustainable pest management strategies.

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.

Heat waves induce milkweed resistance to a specialist herbivore via increased toxicity and reduced nutrient content.

Over the last decade, a large effort has been made to understand how extreme climate events disrupt species interactions. Yet, it is unclear how these events affect plants and herbivores directly, via metabolic changes, and indirectly, via their subsequent altered interaction. We exposed common milkweed (Asclepias syriaca) and monarch caterpillars (Danaus plexippus) to control (26:14°C, day:night) or heat wave (HW) conditions (36:24°C, day:night) for 4 days and then moved each organism to a new control or HW partner to disentangle the direct and indirect effects of heat exposure on each organism. We found that the HW directly benefited plants in terms of growth and defence expression (increased latex exudation and total cardenolides) and insect her'bivores through faster larval development. Conversely, indirect HW effects caused both plant latex and total cardenolides to decrease after subsequent herbivory. Nonetheless, increasing trends of more toxic cardenolides and lower leaf nutritional quality after herbivory by HW caterpillars likely led to reduced plant damage compared to controls. Our findings reveal that indirect impacts of HWs may play a greater role in shaping plant-herbivore interactions via changes in key physiological traits, providing valuable understanding of how ecological interactions may proceed in a changing world.

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.