In many organisms, population-density sensing and sexual attraction rely on small-molecule-based signalling systems1,2. In the nematode Caenorhabditis elegans, population density is monitored through specific glycosides of the dideoxysugar ascarylose (the `ascarosides') that promote entry into an alternative larval stage, the non-feeding and highly persistent dauer stage3,4. In addition, adult C. elegans males are attracted to hermaphrodites by a previously unidentified small-molecule signal5,6. Here we show, by means of combinatorial activity-guided fractionation of the C. elegans metabolome, that the mating signal consists of a synergistic blend of three dauer-inducing ascarosides, which we call ascr#2, ascr#3 and ascr#4. This blend of ascarosides acts as a potent male attractant at very low concentrations, whereas at the higher concentrations required for dauer formation the compounds no longer attract males and instead deter hermaphrodites. The ascarosides ascr#2 and ascr#3 carry different, but overlapping, information, as ascr#3 is more potent as a male attractant than ascr#2, whereas ascr#2 is slightly more potent than ascr#3 in promoting dauer formation7. We demonstrate that ascr#2, ascr#3 and ascr#4 are strongly synergistic, and that two types of neuron, the amphid single-ciliated sensory neuron type K (ASK) and the male-specific cephalic companion neuron (CEM), are required for male attraction by ascr#3. On the basis of these results, male attraction and dauer formation in C. elegans appear as alternative behavioural responses to a common set of signalling molecules. The ascaroside signalling system thus connects reproductive and developmental pathways and represents a unique example of structure- and concentration-dependent differential activity of signalling molecules.
Phytoalexins constitute a broad category of pathogen-and insectinducible biochemicals that locally protect plant tissues. Because of their agronomic significance, maize and rice have been extensively investigated for their terpenoid-based defenses, which include insect-inducible monoterpene and sesquiterpene volatiles. Rice also produces a complex array of pathogen-inducible diterpenoid phytoalexins. Despite the demonstration of fungal-induced entkaur-15-ene production in maize over 30 y ago, the identity of functionally analogous maize diterpenoid phytoalexins has remained elusive. In response to stem attack by the European corn borer (Ostrinia nubilalis) and fungi, we observed the induced accumulation of six ent-kaurane-related diterpenoids, collectively termed kauralexins. Isolation and identification of the predominant Rhizopus microsporus-induced metabolites revealed ent-kaur-19-al-17-oic acid and the unique analog ent-kaur-15-en-19-al-17-oic acid, assigned as kauralexins A3 and B3, respectively. Encoding an entcopalyl diphosphate synthase, fungal-induced An2 transcript accumulation precedes highly localized kauralexin production, which can eventually exceed 100 μg·g −1 fresh weight. Pharmacological applications of jasmonic acid and ethylene also synergize the induced accumulation of kauralexins. Occurring at elevated levels in the scutella of all inbred lines examined, kauralexins appear ubiquitous in maize. At concentrations as low as 10 μg·mL −1 , kauralexin B3 significantly inhibited the growth of the opportunistic necrotroph R. microsporus and the causal agent of anthracnose stalk rot, Colletotrichum graminicola. Kauralexins also exhibited significant O. nubilalis antifeedant activity. Our work establishes the presence of diterpenoid defenses in maize and enables a more detailed analysis of their biosynthetic pathways, regulation, and crop defense function.
Plants can perceive a wide range of biotic attackers and respond with targeted induced defenses. Specificity in plant non-selfrecognition occurs either directly by perception of pest-derived elicitors or indirectly through resistance protein recognition of host targets that are inappropriately proteolyzed. Indirect plant perception can occur during interactions with pathogens, yet evidence for analogous events mediating the detection of insect herbivores remains elusive. Here we report indirect perception of herbivory in cowpea (Vigna unguiculata) plants attacked by fall armyworm (Spodoptera frugiperda) larvae. We isolated and identified a disulfide-bridged peptide ( ؉ ICDINGVCVDA ؊ ), termed inceptin, from S. frugiperda larval oral secretions that promotes cowpea ethylene production at 1 fmol leaf ؊1 and triggers increases in the defenserelated phytohormones salicylic acid and jasmonic acid. Inceptins are proteolytic fragments of chloroplastic ATP synthase ␥-subunit regulatory regions that mediate plant perception of herbivory through the induction of volatile, phenylpropanoid, and protease inhibitor defenses. Only S. frugiperda larvae that previously ingested chloroplastic ATP synthase ␥-subunit proteins and produced inceptins significantly induced cowpea defenses after herbivory. Digestive fragments of an ancient and essential plant enzyme, inceptin functions as a potent indirect signal initiating specific plant responses to insect attack.elicitor ͉ guard hypothesis ͉ indirect perception ͉ insect herbivory ͉ plant defense A mechanistic understanding and targeted improvement of plant resistance traits are recognized as essential in combating yield losses from crop pests. Plants can perceive and defensively respond to attack either directly by impeding pest growth or indirectly by promoting advantageous interactions with beneficial organisms (1-7). Great progress has been made in the identification of plant receptor-like kinase families mediating perception of biotic attack and the subsequent activation of signal transduction cascades spanning interactions of GTP binding proteins, mitogen-activated protein kinases, phytohormones, transcription factors, and ultimately induced biochemical defenses (2,8). Despite these advances, relatively few candidate elicitors and ligands responsible for the initiation and specificity of induced plant defenses to pest attack have been identified (1, 2). This void is especially acute in the case of insect herbivore perception and is surprising given both the significance of plant-insect interactions in arthropod and angiosperm evolution and the role of insects in facilitating plant pathogen entry (9, 10).Induced plant defenses are initiated in part by the direct perception of elicitors derived from offending organisms. For example, maize (Zea mays) and tobacco (Nicotiana attenuata) perceive insect attack through the direct detection of fatty acid amino acid conjugate (FAC) elicitors present in insect oral secretions (OS). Plants respond with indirect defenses in the form of indu...
Nonvolatile terpenoid phytoalexins occur throughout the plant kingdom, but until recently were not known constituents of chemical defense in maize (Zea mays). We describe a novel family of ubiquitous maize sesquiterpenoid phytoalexins, termed zealexins, which were discovered through characterization of Fusarium graminearum-induced responses. Zealexins accumulate to levels greater than 800 μg g−1 fresh weight in F. graminearum-infected tissue. Their production is also elicited by a wide variety of fungi, Ostrinia nubilalis herbivory, and the synergistic action of jasmonic acid and ethylene. Zealexins exhibit antifungal activity against numerous phytopathogenic fungi at physiologically relevant concentrations. Structural elucidation of four members of this complex family revealed that all are acidic sesquiterpenoids containing a hydrocarbon skeleton that resembles β-macrocarpene. Induced zealexin accumulation is preceded by increased expression of the genes encoding TERPENE SYNTHASE6 (TPS6) and TPS11, which catalyze β-macrocarpene production. Furthermore, zealexin accumulation displays direct positive relationships with the transcript levels of both genes. Microarray analysis of F. graminearum-infected tissue revealed that Tps6/Tps11 were among the most highly up-regulated genes, as was An2, an ent-copalyl diphosphate synthase associated with production of kauralexins. Transcript profiling suggests that zealexins cooccur with a number of antimicrobial proteins, including chitinases and pathogenesis-related proteins. In addition to zealexins, kauralexins and the benzoxazinoid 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one-glucose (HDMBOA-glucose) were produced in fungal-infected tissue. HDMBOA-glucose accumulation occurred in both wild-type and benzoxazine-deficient1 (bx1) mutant lines, indicating that Bx1 gene activity is not required for HDMBOA biosynthesis. Together these results indicate an important cooperative role of terpenoid phytoalexins in maize biochemical defense.
Insect-induced defenses occur in nearly all plants and are regulated by conserved signaling pathways. As the first described plant peptide signal, systemin regulates antiherbivore defenses in the Solanaceae, but in other plant families, peptides with analogous activity have remained elusive. In the current study, we demonstrate that a member of the maize ( Zea mays ) plant elicitor peptide (Pep) family, ZmPep3, regulates responses against herbivores. Consistent with being a signal, expression of the ZmPROPEP3 precursor gene is rapidly induced by Spodoptera exigua oral secretions. At concentrations starting at 5 pmol per leaf, ZmPep3 stimulates production of jasmonic acid, ethylene, and increased expression of genes encoding proteins associated with herbivory defense. These include proteinase inhibitors and biosynthetic enzymes for production of volatile terpenes and benzoxazinoids. In accordance with gene expression data, plants treated with ZmPep3 emit volatiles similar to those from plants subjected to herbivory. ZmPep3-treated plants also exhibit induced accumulation of the benzoxazinoid phytoalexin 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside. Direct and indirect defenses induced by ZmPep3 contribute to resistance against S. exigua through significant reduction of larval growth and attraction of Cotesia marginiventris parasitoids. ZmPep3 activity is specific to Poaceous species; however, peptides derived from PROPEP orthologs identified in Solanaceous and Fabaceous plants also induce herbivory-associated volatiles in their respective species. These studies demonstrate that Peps are conserved signals across diverse plant families regulating antiherbivore defenses and are likely to be the missing functional homologs of systemin outside of the Solanaceae.
In response to insect attack, many plants exhibit dynamic biochemical changes, resulting in the induced production of direct and indirect defenses. Elicitors present in herbivore oral secretions are believed to positively regulate many inducible plant defenses; however, little is known about the specificity of elicitor recognition in plants. To investigate the phylogenic distribution of elicitor activity, we tested representatives from three different elicitor classes on the time course of defense-related phytohormone production, including ethylene (E), jasmonic acid (JA), and salicylic acid, in a range of plant species spanning angiosperm diversity. All families examined responded to at least one elicitor class with significant increases in E and JA production within 1 to 2 h after treatment, yet elicitation activity among species was highly idiosyncratic. The fatty-acid amino acid conjugate volicitin exhibited the widest range of phytohormone and volatile inducing activity, which spanned maize (Zea mays), soybean (Glycine max), and eggplant (Solanum melongena). In contrast, the activity of inceptinrelated peptides, originally described in cowpea (Vigna unguiculata), was limited even within the Fabaceae. Similarly, caeliferin A16:0, a disulfooxy fatty acid from grasshoppers, was the only elicitor with demonstrable activity in Arabidopsis thaliana. Although precise mechanisms remain unknown, the unpredictable nature of elicitor activity between plant species supports the existence of specific receptor-ligand interactions mediating recognition. Despite the lack of an ideal plant model for studying the action of numerous elicitors, E and JA exist as highly conserved and readily quantifiable markers for future discoveries in this field.ethylene ͉ insect elicitor ͉ jasmonic acid ͉ plant defense ͉ volatile organic compound
It has long been proposed that the nominal species Anastrepha fraterculus is a species complex and earlier studies showed high levels of pre-zygotic isolation between two laboratory strains from Argentina and Peru. Further experiments were carried out on the same populations and on their reciprocal hybrids, including pre-and post-zygotic isolation studies, pheromone analysis, and mitotic and polytene chromosome analysis. A high level of pre-zygotic isolation had been maintained between the parental strains despite 3 years of laboratory rearing under identical conditions. The level of pre-zygotic isolation was reduced in matings with hybrids. There were also differences in other components of mating behaviour. There were quantitative and qualitative differences in the sex pheromone of the two strains with the hybrids producing a mixture. The pre-zygotic isolation barriers were complemented by high levels of post-zygotic inviability and sex ratio distortion, most likely not due to Wolbachia, although there was evidence of some cytoplasmic factor involved in sex ratio distortion. Analysis of polytene chromosomes revealed a high level of asynapsis in the hybrids, together with karyotypic differences between the parental strains. The combined results of the present study indicate that these two strains belong to different biological entities within the proposed A. fraterculus complex.
BackgroundSugar feeding is critical for survival of malaria vectors and, although discriminative plant feeding previously has been shown to occur in Anopheles gambiae s.s., little is known about the cues mediating attraction to these plants. In this study, we investigated the role of olfaction in An. gambiae discriminative feeding behaviour.MethodsDual choice olfactometer assays were used to study odour discrimination by An. gambiae to three suspected host plants: Parthenium hysterophorus (Asteraceae), Bidens pilosa (Asteraceae) and Ricinus communis (Euphorbiaceae). Sugar content of the three plant species was determined by analysis of their trimethylsilyl derivatives by coupled gas chromatography–mass spectrometry (GC-MS) and confirmed with authentic standards. Volatiles from intact plants of the three species were collected on Super Q and analyzed by coupled GC-electroantennographic detection (GC-EAD) and GC-MS to identify electrophysiologically-active components whose identities were also confirmed with authentic standards. Active compounds and blends were formulated using dose–response olfactory bioassays. Responses of females were converted into preference indices and analyzed by chi-square tests. The amounts of common behaviourally-active components released by the three host plants were compared with one-way ANOVA.ResultsOverall, the sugar contents were similar in the two Asteraceae plants, P. hysterophorus and B. pilosa, but richer in R. communis. Odours released by P. hysterophorus were the most attractive, with those from B. pilosa being the least attractive to females in the olfactometer assays. Six EAD-active components identified were consistently detected by the antennae of adult females. The amounts of common antennally-active components released varied with the host plant, with the highest amounts released by P. hysterophorus. In dose–response assays, single compounds and blends of these components were attractive to females but to varying levels, with one of the blends recording a significantly attractive response from females when compared to volatiles released by either the most preferred plant, P. hysterophorus (χ2 = 5.23, df = 1, P < 0.05) or as a synthetic blend mimicking that released by P. hysterophorus.ConclusionsOur results demonstrate that (a) a specific group of plant odours attract female An. gambiae (b) females use both qualitative and quantitative differences in volatile composition to associate and discriminate between different host plants, and (c) altering concentrations of individual EAD-active components in a blend provides a practical direction for developing effective plant-based lures for malaria vector management.
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