Odorant detection in a locust exhibits unusually low redundancy.

Olfactory coding, from insects to humans, is canonically considered to involve considerable across-fiber coding already at the peripheral level, thereby allowing recognition of vast numbers of odor compounds. We show that the migratory locust has evolved an alternative strategy built on highly specific odorant receptors feeding into a complex primary processing center in the brain. By collecting odors from food and different life stages of the locust, we identified 205 ecologically relevant odorants, which we used to deorphanize 48 locust olfactory receptors via ectopic expression in Drosophila. Contrary to the often broadly tuned olfactory receptors of other insects, almost all locust receptors were found to be narrowly tuned to one or very few ligands. Knocking out a single receptor using CRISPR abolished physiological and behavioral responses to the corresponding ligand. We conclude that the locust olfactory system, with most olfactory receptors being narrowly tuned, differs from the so-far described olfactory systems.

Role of jasmonate signaling in rice resistance to the leaf folder Cnaphalocrocis medinalis.

KEY MESSAGE: Jasmonate-induced accumulation of anti-herbivore compounds mediates rice resistance to the leaf folder Cnaphalocrocis medinalis. The rice leaf folder (LF), Cnaphalocrocis medinalis, is one of the most destructive insect pests in the paddy field. LF larvae induces leaf folding and scrapes the upper epidermis and mesophyll tissues reducing photosynthesis and yield in rice. Identifying plant defense pathways and genes involved in LF resistance is essential to understand better this plant-insect interaction and develop new control strategies for this pest. Jasmonate (JA) signaling controls a plethora of plant defenses against herbivores. Using RNA-seq time series analysis, we characterized changes in the transcriptome of wild-type (WT) leaves in response to LF damage and measured the dynamics of accumulation of JA phytohormone pools in time-course experiments. Genes related to JA signaling and responses, known to mediate resistance responses to herbivores, were induced by LF and were accompanied by an increment in the levels of JA pools in damaged leaves. The accumulation of defense compounds such as phenolamides and trypsin proteinase inhibitor (TPI) also increased after LF infestation in WT but not in JA mutant plants impaired in JA biosynthesis (aoc-2) and signaling (myc2-5). Consistent with all these responses, we found that LF larvae performed better in the JA mutant backgrounds than in the WT plants. Our results show that JA signaling regulates LF-induced accumulation of TPI and phenolamides and that these compounds are likely an essential part of the defense arsenal of rice plants against this insect pest.

Specific decorations of 17-hydroxygeranyllinalool diterpene glycosides solve the autotoxicity problem of chemical defense in Nicotiana attenuata.

The native diploid tobacco Nicotiana attenuata produces abundant, potent anti-herbivore defense metabolites known as 17-hydroxygeranyllinalool diterpene glycosides (HGL-DTGs) whose glycosylation and malonylation biosynthetic steps are regulated by jasmonate signaling. To characterize the biosynthetic pathway of HGL-DTGs, we conducted a genome-wide analysis of uridine diphosphate glycosyltransferases (UGTs) and identified 107 family-1 UGT members. The transcript levels of three UGTs were highly correlated with the transcript levels two key HGL-DTG biosynthetic genes: geranylgeranyl diphosphate synthase (NaGGPPS) and geranyllinalool synthase (NaGLS). NaGLS's role in HGL-DTG biosynthesis was confirmed by virus-induced gene silencing. Silencing the Uridine diphosphate (UDP)-rhamnosyltransferase gene UGT91T1 demonstrated its role in the rhamnosylation of HGL-DTGs. In vitro enzyme assays revealed that UGT74P3 and UGT74P4 use UDP-glucose for the glucosylation of 17-hydroxygeranyllinalool (17-HGL) to lyciumoside I. Plants with stable silencing of UGT74P3 and UGT74P5 were severely developmentally deformed, pointing to a phytotoxic effect of the aglycone. The application of synthetic 17-HGL and silencing of the UGTs in HGL-DTG-free plants confirmed this phytotoxic effect. Feeding assays with tobacco hornworm (Manduca sexta) larvae revealed the defensive functions of the glucosylation and rhamnosylation steps in HGL-DTG biosynthesis. Glucosylation of 17-HGL is therefore a critical step that contributes to the resulting metabolites' defensive function and solves the autotoxicity problem of this potent chemical defense.

ZEITLUPE in the Roots of Wild Tobacco Regulates Jasmonate-Mediated Nicotine Biosynthesis and Resistance to a Generalist Herbivore.

The jasmonate (JA) phytohormone signaling system is an important mediator of plant defense against herbivores. Plants deficient in JA signaling are more susceptible to herbivory as a result of deficiencies in defensive trait expression. Recent studies have implicated the circadian clock in regulating JA-mediated defenses, but the molecular mechanisms linking the clock to JA signaling are unclear. Here, we report that wild tobacco (Nicotiana attenuata) plants rendered deficient in the clock component ZEITLUPE (ZTL) by RNA interference have attenuated resistance to the generalist herbivore Spodoptera littoralis This effect can be attributed in part to reduced concentrations of nicotine, an abundant JA-regulated toxin produced in N. attenuata roots and transported to shoots. RNA interference targeting ZTL dramatically affects the root circadian clock and reduces the expression of nicotine biosynthetic genes. Protein-protein interaction experiments demonstrate that ZTL regulates JA signaling by directly interacting with JASMONATE ZIM domain (JAZ) proteins in a CORONATINE-INSENSITIVE1- and jasmonoyl-isoleucine conjugate-independent manner, thereby regulating a JAZ-MYC2 module that is required for nicotine biosynthesis. Our study reveals new functions for ZTL and proposes a mechanism by which a clock component directly influences JA signaling to regulate plant defense against herbivory.

Jasmonate signaling makes flowers attractive to pollinators and repellant to florivores in nature.

Flowers are required for the Darwinian fitness of flowering plants, but flowers' advertisements for pollination services can attract florivores. Previous glasshouse work with Nicotiana attenuata revealed the role of jasmonate (JA) signaling in flower development, advertisement and defense. However, whether JA signaling mediates flowers' filtering of floral visitors in nature remained unknown. This field study revealed that silencing JA signaling resulted in flowers that produce less nectar and benzyl acetone, two pollinator-attractive traits. Meanwhile, flowers of defenseless plants were highly attacked by a suite of native herbivores, and damage to buds in native plants correlated negatively with their JA-Ile levels.