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.

Neofunctionalization of Toll Signaling in Insects: From Immunity to Dorsoventral Patterning.

Toll signaling plays a crucial role in pathogen defense throughout the animal kingdom. It was discovered, however, for its function in dorsoventral (DV) axis formation in Drosophila. In all other insects studied so far, but not outside the insects, Toll is also required for DV patterning. However, in insects more distantly related to Drosophila, Toll's patterning role is frequently reduced and substituted by an expanded influence of BMP signaling, the pathway implicated in DV axis formation in all major metazoan lineages. This suggests that Toll was integrated into an ancestral BMP-based patterning system at the base of the insects or during insect evolution. The observation that Toll signaling has an immune function in the extraembryonic serosa, an early differentiating tissue of most insect embryos, suggests a scenario of how Toll was co-opted from an ancestral immune function for its new role in axis formation.

Parasitic modulation of host development by ubiquitin-independent protein degradation.

Certain obligate parasites induce complex and substantial phenotypic changes in their hosts in ways that favor their transmission to other trophic levels. However, the mechanisms underlying these changes remain largely unknown. Here we demonstrate how SAP05 protein effectors from insect-vectored plant pathogenic phytoplasmas take control of several plant developmental processes. These effectors simultaneously prolong the host lifespan and induce witches' broom-like proliferations of leaf and sterile shoots, organs colonized by phytoplasmas and vectors. SAP05 acts by mediating the concurrent degradation of SPL and GATA developmental regulators via a process that relies on hijacking the plant ubiquitin receptor RPN10 independent of substrate ubiquitination. RPN10 is highly conserved among eukaryotes, but SAP05 does not bind insect vector RPN10. A two-amino-acid substitution within plant RPN10 generates a functional variant that is resistant to SAP05 activities. Therefore, one effector protein enables obligate parasitic phytoplasmas to induce a plethora of developmental phenotypes in their hosts.

An Affair to Remember: How an Endosymbiont Partners with Its Host to Build a Cell Envelope.

Studying endosymbionts gives us insight into early cellular mechanisms that led to the emergence of eukaryotic organelles. In this issue of Cell, Bublitz et al. (2019) report on how a nested bacterial endosymbiont of mealybugs builds its cell wall peptidoglycan through a biosynthetic pathway that is dependent on transported host enzymes.

Crystal Structure of the COMPASS H3K4 Methyltransferase Catalytic Module.

The SET1/MLL family of histone methyltransferases is conserved in eukaryotes and regulates transcription by catalyzing histone H3K4 mono-, di-, and tri-methylation. These enzymes form a common five-subunit catalytic core whose assembly is critical for their basal and regulated enzymatic activities through unknown mechanisms. Here, we present the crystal structure of the intact yeast COMPASS histone methyltransferase catalytic module consisting of Swd1, Swd3, Bre2, Sdc1, and Set1. The complex is organized by Swd1, whose conserved C-terminal tail not only nucleates Swd3 and a Bre2-Sdc1 subcomplex, but also joins Set1 to construct a regulatory pocket next to the catalytic site. This inter-subunit pocket is targeted by a previously unrecognized enzyme-modulating motif in Swd3 and features a doorstop-style mechanism dictating substrate selectivity among SET1/MLL family members. By spatially mapping the functional components of COMPASS, our results provide a structural framework for understanding the multifaceted functions and regulation of the H3K4 methyltransferase family.

Structure and Conformational Dynamics of a COMPASS Histone H3K4 Methyltransferase Complex.

The methylation of histone 3 lysine 4 (H3K4) is carried out by an evolutionarily conserved family of methyltransferases referred to as complex of proteins associated with Set1 (COMPASS). The activity of the catalytic SET domain (su(var)3-9, enhancer-of-zeste, and trithorax) is endowed through forming a complex with a set of core proteins that are widely shared from yeast to humans. We obtained cryo-electron microscopy (cryo-EM) maps of the yeast Set1/COMPASS core complex at overall 4.0- to 4.4-Å resolution, providing insights into its structural organization and conformational dynamics. The Cps50 C-terminal tail weaves within the complex to provide a central scaffold for assembly. The SET domain, snugly positioned at the junction of the Y-shaped complex, is extensively contacted by Cps60 (Bre2), Cps50 (Swd1), and Cps30 (Swd3). The mobile SET-I motif of the SET domain is engaged by Cps30, explaining its key role in COMPASS catalytic activity toward higher H3K4 methylation states.

Structural Basis for Teneurin Function in Circuit-Wiring: A Toxin Motif at the Synapse.

Teneurins (TENs) are cell-surface adhesion proteins with critical roles in tissue development and axon guidance. Here, we report the 3.1-Å cryoelectron microscopy structure of the human TEN2 extracellular region (ECR), revealing a striking similarity to bacterial Tc-toxins. The ECR includes a large ß barrel that partially encapsulates a C-terminal domain, which emerges to the solvent through an opening in the mid-barrel region. An immunoglobulin (Ig)-like domain seals the bottom of the barrel while a ß propeller is attached in a perpendicular orientation. We further show that an alternatively spliced region within the ß propeller acts as a switch to regulate trans-cellular adhesion of TEN2 to latrophilin (LPHN), a transmembrane receptor known to mediate critical functions in the central nervous system. One splice variant activates trans-cellular signaling in a LPHN-dependent manner, whereas the other induces inhibitory postsynaptic differentiation. These results highlight the unusual structural organization of TENs giving rise to their multifarious functions.

Big Role for a Tiny Genome.

In this issue of Cell, Salem et al. demonstrate a remarkable instance of herbivory dependent on a co-evolved mutualism with specialized bacteria. Despite having a tiny genome and limited metabolic repertoire, the bacteria in Cassida beetles produce pectinases predicted to mediate degradation of plant cell walls in the insect diet.

The MutAnts Are Here.

The development of CRISPR/Cas9-mediated gene knockout in two ant species opens a new window into exploring how social insects use olfactory cues to organize their collective behavior.

Ecology and Evolution of Communication in Social Insects.

Insect life strategies comprise all levels of sociality from solitary to eusocial, in which individuals form persistent groups and divide labor. With increasing social complexity, the need to communicate a greater diversity of messages arose to coordinate division of labor, group cohesion, and concerted actions. Here we summarize the knowledge on prominent messages in social insects that inform about reproduction, group membership, resource locations, and threats and discuss potential evolutionary trajectories of each message in the context of social complexity.

Disproportionate declines of formerly abundant species underlie insect loss.

Studies have reported widespread declines in terrestrial insect abundances in recent years1-4, but trends in other biodiversity metrics are less clear-cut5-7. Here we examined long-term trends in 923 terrestrial insect assemblages monitored in 106 studies, and found concomitant declines in abundance and species richness. For studies that were resolved to species level (551 sites in 57 studies), we observed a decline in the number of initially abundant species through time, but not in the number of very rare species. At the population level, we found that species that were most abundant at the start of the time series showed the strongest average declines (corrected for regression-to-the-mean effects). Rarer species were, on average, also declining, but these were offset by increases of other species. Our results suggest that the observed decreases in total insect abundance2 can mostly be explained by widespread declines of formerly abundant species. This counters the common narrative that biodiversity loss is mostly characterized by declines of rare species8,9. Although our results suggest that fundamental changes are occurring in insect assemblages, it is important to recognize that they represent only trends from those locations for which sufficient long-term data are available. Nevertheless, given the importance of abundant species in ecosystems10, their general declines are likely to have broad repercussions for food webs and ecosystem functioning.

Weather explains the decline and rise of insect biomass over 34 years.

Insects have a pivotal role in ecosystem function, thus the decline of more than 75% in insect biomass in protected areas over recent decades in Central Europe1 and elsewhere2,3 has alarmed the public, pushed decision-makers4 and stimulated research on insect population trends. However, the drivers of this decline are still not well understood. Here, we reanalysed 27 years of insect biomass data from Hallmann et al.1, using sample-specific information on weather conditions during sampling and weather anomalies during the insect life cycle. This model explained variation in temporal decline in insect biomass, including an observed increase in biomass in recent years, solely on the basis of these weather variables. Our finding that terrestrial insect biomass is largely driven by complex weather conditions challenges previous assumptions that climate change is more critical in the tropics5,6 or that negative consequences in the temperate zone might only occur in the future7. Despite the recent observed increase in biomass, new combinations of unfavourable multi-annual weather conditions might be expected to further threaten insect populations under continuing climate change. Our findings also highlight the need for more climate change research on physiological mechanisms affected by annual weather conditions and anomalies.

Interactive features of proteins composing eukaryotic circadian clocks.

Research into the molecular mechanisms of eukaryotic circadian clocks has proceeded at an electrifying pace. In this review, we discuss advances in our understanding of the structures of central molecular players in the timing oscillators of fungi, insects, and mammals. A series of clock protein structures demonstrate that the PAS (Per/Arnt/Sim) domain has been used with great variation to formulate the transcriptional activators and repressors of the clock. We discuss how posttranslational modifications and external cues, such as light, affect the conformation and function of core clock components. Recent breakthroughs have also revealed novel interactions among clock proteins and new partners that couple the clock to metabolic and developmental pathways. Overall, a picture of clock function has emerged wherein conserved motifs and structural platforms have been elaborated into a highly dynamic collection of interacting molecules that undergo orchestrated changes in chemical structure, conformational state, and partners.

Bridging two insect flight modes in evolution, physiology and robophysics.

Since taking flight, insects have undergone repeated evolutionary transitions between two seemingly distinct flight modes1-3. Some insects neurally activate their muscles synchronously with each wingstroke. However, many insects have achieved wingbeat frequencies beyond the speed limit of typical neuromuscular systems by evolving flight muscles that are asynchronous with neural activation and activate in response to mechanical stretch2-8. These modes reflect the two fundamental ways of generating rhythmic movement: time-periodic forcing versus emergent oscillations from self-excitation8-10. How repeated evolutionary transitions have occurred and what governs the switching between these distinct modes remain unknown. Here we find that, despite widespread asynchronous actuation in insects across the phylogeny3,6, asynchrony probably evolved only once at the order level, with many reversions to the ancestral, synchronous mode. A synchronous moth species, evolved from an asynchronous ancestor, still preserves the stretch-activated muscle physiology. Numerical and robophysical analyses of a unified biophysical framework reveal that rather than a dichotomy, these two modes are two regimes of the same dynamics. Insects can transition between flight modes across a bridge in physiological parameter space. Finally, we integrate these two actuation modes into an insect-scale robot11-13 that enables transitions between modes and unlocks a new self-excited wingstroke strategy for engineered flight. Together, this framework accounts for repeated transitions in insect flight evolution and shows how flight modes can flip with changes in physiological parameters.

Effects of moisture and density-dependent interactions on tropical tree diversity.

Tropical tree diversity increases with rainfall1,2. Direct physiological effects of moisture availability and indirect effects mediated by biotic interactions are hypothesized to contribute to this pantropical increase in diversity with rainfall2-6. Previous studies have demonstrated direct physiological effects of variation in moisture availability on tree survival and diversity5,7-10, but the indirect effects of variation in moisture availability on diversity mediated by biotic interactions have not been shown11. Here we evaluate the relationships between interannual variation in moisture availability, the strength of density-dependent interactions, and seedling diversity in central Panama. Diversity increased with soil moisture over the first year of life across 20 annual cohorts. These first-year changes in diversity persisted for at least 15 years. Differential survival of moisture-sensitive species did not contribute to the observed changes in diversity. Rather, negative density-dependent interactions among conspecifics were stronger and increased diversity in wetter years. This suggests that moisture availability enhances diversity indirectly through moisture-sensitive, density-dependent conspecific interactions. Pathogens and phytophagous insects mediate interactions among seedlings in tropical forests12-18, and many of these plant enemies are themselves moisture-sensitive19-27. Changes in moisture availability caused by climate change and habitat degradation may alter these interactions and tropical tree diversity.

Genetic basis of chemical communication in eusocial insects.

Social behavior is one of the most fascinating and complex behaviors in humans and animals. A fundamental process of social behavior is communication among individuals. It relies on the capability of the nervous system to sense, process, and interpret various signals (e.g., pheromones) and respond with appropriate decisions and actions. Eusocial insects, including ants, some bees, some wasps, and termites, display intriguing cooperative social behavior. Recent advances in genetic and genomic studies have revealed key genes that are involved in pheromone synthesis, chemosensory perception, and physiological and behavioral responses to varied pheromones. In this review, we highlight the genes and pathways that regulate queen pheromone-mediated social communication, discuss the evolutionary changes in genetic systems, and outline prospects of functional studies in sociobiology.

Competition for pollinators destabilizes plant coexistence.

Mounting concern over the global decline of pollinators has fuelled calls for investigating their role in maintaining plant diversity1,2. Theory predicts that competition for pollinators can stabilize interactions between plant species by providing opportunities for niche differentiation3, while at the same time can drive competitive imbalances that favour exclusion4. Here we empirically tested these contrasting effects by manipulating competition for pollinators in a way that predicts its long-term implications for plant coexistence. We subjected annual plant individuals situated across experimentally imposed gradients in neighbour density to either ambient insect pollination or a pollen supplementation treatment alleviating competition for pollinators. The vital rates of these individuals informed plant population dynamic models predicting the key theoretical metrics of species coexistence. Competition for pollinators generally destabilized the interactions between plant species, reducing the proportion of pairs expected to coexist. Interactions with pollinators also influenced the competitive imbalances between plant species, effects that are expected to strengthen with pollinator decline, potentially disrupting plant coexistence. Indeed, results from an experiment simulating pollinator decline showed that plant species experiencing greater reductions in floral visitation also suffered greater declines in population growth rate. Our results reveal that competition for pollinators may weaken plant coexistence by destabilizing interactions and contributing to competitive imbalances, information critical for interpreting the impacts of pollinator decline.

Agriculture and climate change are reshaping insect biodiversity worldwide.

Several previous studies have investigated changes in insect biodiversity, with some highlighting declines and others showing turnover in species composition without net declines1-5. Although research has shown that biodiversity changes are driven primarily by land-use change and increasingly by climate change6,7, the potential for interaction between these drivers and insect biodiversity on the global scale remains unclear. Here we show that the interaction between indices of historical climate warming and intensive agricultural land use is associated with reductions of almost 50% in the abundance and 27% in the number of species within insect assemblages relative to those in less-disturbed habitats with lower rates of historical climate warming. These patterns are particularly evident in the tropical realm, whereas some positive responses of biodiversity to climate change occur in non-tropical regions in natural habitats. A high availability of nearby natural habitat often mitigates reductions in insect abundance and richness associated with agricultural land use and substantial climate warming but only in low-intensity agricultural systems. In such systems, in which high levels (75% cover) of natural habitat are available, abundance and richness were reduced by 7% and 5%, respectively, compared with reductions of 63% and 61% in places where less natural habitat is present (25% cover). Our results show that insect biodiversity will probably benefit from mitigating climate change, preserving natural habitat within landscapes and reducing the intensity of agriculture.

Accommodating unobservability to control flight attitude with optic flow.

Attitude control is an essential flight capability. Whereas flying robots commonly rely on accelerometers1 for estimating attitude, flying insects lack an unambiguous sense of gravity2,3. Despite the established role of several sense organs in attitude stabilization3-5, the dependence of flying insects on an internal gravity direction estimate remains unclear. Here we show how attitude can be extracted from optic flow when combined with a motion model that relates attitude to acceleration direction. Although there are conditions such as hover in which the attitude is unobservable, we prove that the ensuing control system is still stable, continuously moving into and out of these conditions. Flying robot experiments confirm that accommodating unobservability in this manner leads to stable, but slightly oscillatory, attitude control. Moreover, experiments with a bio-inspired flapping-wing robot show that residual, high-frequency attitude oscillations from flapping motion improve observability. The presented approach holds a promise for robotics, with accelerometer-less autopilots paving the road for insect-scale autonomous flying robots6. Finally, it forms a hypothesis on insect attitude estimation and control, with the potential to provide further insight into known biological phenomena5,7,8 and to generate new predictions such as reduced head and body attitude variance at higher flight speeds9.

Acoustic Pattern Recognition and Courtship Songs: Insights from Insects.

Across the animal kingdom, social interactions rely on sound production and perception. From simple cricket chirps to more elaborate bird songs, animals go to great lengths to communicate information critical for reproduction and survival via acoustic signals. Insects produce a wide array of songs to attract a mate, and the intended receivers must differentiate these calls from competing sounds, analyze the quality of the sender from spectrotemporal signal properties, and then determine how to react. Insects use numerically simple nervous systems to analyze and respond to courtship songs, making them ideal model systems for uncovering the neural mechanisms underlying acoustic pattern recognition. We highlight here how the combination of behavioral studies and neural recordings in three groups of insects-crickets, grasshoppers, and fruit flies-reveals common strategies for extracting ethologically relevant information from acoustic patterns and how these findings might translate to other systems.