Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata

Flowers produce a plethora of secondary metabolites but only nectar sugars, floral pigments and headspace volatiles have been examined in the context of pollinator behavior. We identify secondary metabolites in the headspace and nectar of glasshouse- and field-grown Nicotiana attenuata plants, infer within-flower origins by analyzing six flower parts, and compare the attractiveness of 16 constituents in standardized choice tests with two guilds of natural pollinators (Manducasexta moths and Archilochus alexandri and Selasphorus rufus hummingbirds) and one nectar thief (Solenopsis xyloni ants) to determine whether nectar metabolites can 'filter' flower visitors: only two could. Moths responded more strongly than did hummingbirds to headspace presentation of nicotine and benzylacetone, the most abundant repellent and attractant compounds, respectively. For both pollinators, nectar repellents decreased nectaring time and nectar volume removed, but increased visitation number, particularly for hummingbirds. Fewer ants visited if the nectar contained repellents. To determine whether nicotine reduced nectar removal rates in nature, we planted transformed, nicotine-silenced plants into native populations in Utah over 2 years. Plants completely lacking nicotine in their nectar had 68-70% more nectar removed per night by the native community of floral visitors than did wild-type plants. We hypothesize that nectar repellents optimize the number of flower visitors per volume of nectar produced, allowing plants to keep their nectar volumes small.     

昆虫共生菌的次级代谢产物研究进展

微生物与昆虫的共生是一种普遍现象,昆虫种类繁多,与昆虫共生的微生物也多种多样。昆虫共生菌是活性次生代谢产物的重要来源。本文对自2008年以来已报道的177个昆虫共生菌的次级代谢产物进行了统计和分析,结果表明:61.6%的化合物为新天然产物(生物碱类新化合物最多),其中,约75%的新化合物来源于昆虫共生真菌,25%来源于细菌;醌酮类化合物是昆虫共生菌源天然产物的主要结构类型,占23.2%;47.5%的化合物具有显著的抗肿瘤、抗菌、除草和抗氧化等生物活性,且化合物中的主要活性类型是抗菌和抗肿瘤活性,活性范围覆盖面最广的结构类型是生物碱类。以上结果表明昆虫共生菌的次级代谢产物是先导性化合物的重要来源且具有丰富的生物活性类型。本文以天然产物的结构分类为切入点,结合其研究菌株来源、生物活性等进行综述,旨在为充分挖掘昆虫共生菌次级代谢产物提供重要参考。     

Mechanisms of resistance to self-produced toxic secondary metabolites in plants

Plants produce a variety of secondary metabolites to protect themselves from pathogens and herbivores and/or to influence the growth of neighbouring plants. Some of these metabolites are toxic to the producing cells when their target sites are present in the producing organisms. Therefore, a specific self-resistance mechanism must exist in these plants. Self-resistance mechanisms, including extracellular excretion, vacuolar sequestration, vesicle transport, extracellular biosynthesis, and accumulation of the metabolite in a non-toxic form, have been proposed thus far. Recently, a new mechanism involving mutation of the target protein of the toxic metabolite has been elucidated. We review here the mechanisms that plants use to prevent self-toxicity from the following representative compounds: cannabinoids, flavonoids, diterpene sclareol, alkaloids, benzoxazinones, phenylpropanoids, cyanogenic glycosides, and glucosinolates.     

Evolutionary basis and ecological role of toxic microbial secondary metabolites

This presentation develops a theory of the evolutionary origin and ecological implications of toxic microbial secondary metabolites. The theory is based on a model system that outlines cause—effect associations between pertinent biotypes in the aflatoxin contamination of developing maize kernels. The model suggests that the aflatoxin-producing fungi are natural digestive tract inhabitants of a number of insect species that feed on developing kernels. During feeding, the insect larvae introduce fungal propagules and provide infection sites on damaged kernels. The fungal association with insects exhibits extraordinary variability, ranging from symbiotic to pathogenic. Elaboration of aflatoxin by the fungus facilitates the pathogenic process in host insects. The theory contends that genetic information for secondary microbial metabolites evolved during ecosystem disequilibria. During periods of ecological stability, mechanisms evolved for repression of toxic secondary metabolite biosynthesis. The theory broadly suggests that contemporary agricultural activities presents the requisite milieu for production or toxic microbial secondary metabolites.     

华北蜜粉源植物的研究*

在调查、收集、整理的基础上,初步筛选出蜜粉源植物 1 176 种及变种,隶属于 106 科 426 属,以刺槐、枣树、荆条、油菜等植物组成主要蜜源。华北是我国重要商品蜜生产基地。最后对华北地区蜜粉源植物的开发利用与保护提出了建议。     

Amygdalin in almond nectar and pollen – facts and possible roles

 Nectar and pollen within flowers are usually the primary attractants to floral visitors. Chemical analysis of almond nectar and pollen in this study revealed that they contain the secondary compound amygdalin. Floral display often reflects pollinator characters, and almond flowers are accordingly designated as “bee flowers”. A previous study in Israel showed that when almonds bloom early in the season they attract honeybees, but later in the season the bees shift toward other species that start blooming. In this study, we offered honeybees sugar solutions containing various concentrations of amygdalin. These preference experiments revealed that in mid-summer bees were not selective, whereas early in the summer they were more discriminating, and consumed faster the sugar solutions with the lower amygdalin concentrations. Possible roles of amygdalin in almond nectar and pollen are discussed. Received September 10, 2002; accepted January 17, 2003 Published online: June 2, 2003     

Insecticidal and insect growth regulatory activities of secondary metabolites from entomopathogenic fungi,Lecanicillium attenuatum

Insect growth regulators (IGRs) are effective alternatives to chemical insecticides because of their specificity and low environmental toxicity. Entomopathogenic fungi are an important natural pathogen of insects and have been developed as biological control agents. They produce a wide range of secondary metabolites such as antibiotics, pesticides, growth-promoting or inhibiting compounds and insect attracting agents. In this study, to explore novel IGR substances from entomopathogenic fungi, culture extracts of 189 entomopathogenic fungi isolated from Korean soil samples were investigated for their juvenile hormone (JH)-based IGR activities. Whereas none of the culture extracts exhibited JH agonist (JHA) activity, 14 extracts showed high levels of JH antagonist (JHAN) activity. Among them, culture extract of JEF-145 strain, which was identified as Lecanicillium attenuatum, showed the highest insecticidal against Aedes albopictus and Plutella xylostella. At liquid culture condition, JHAN activity was observed in culture soup rather than mycelial cake, indicating that substances with JHAN activity are released from the JEF-145 strain during culture. Furthermore, while extract from solid cultured JEF-145 strain showed insecticidal activities against both A. albopictus and P. xylostella, that from liquid cultured fungi showed insecticidal activity only against A. albopictus, indicating that L. attenuatum JEF-145 strain produces different kinds of secondary metabolites with JHAN activity depending on culture conditions. These results suggested that JHAN substances derived from entomopathogenic fungi could be usefully exploited to develop novel eco-friendly IGR insecticides.     

The effects of insect visitors on nectar constituents in temperate plants

Summary The floral nectar of angiosperms is primarily a solution of simple sugars, but contains detectable amounts of other solutes, particularly amino acids. These have been regarded as diagnostic, for phylogenetic and taxonomic purposes, and their mean concentrations may be significant in relation to the pollination syndrome of a plant species. However, in several temperate flowers the amino acid concentration varied by an order of magnitude when measured at intervals through a single day. In open, cup-shaped flowers, this was partly due to post-secretory equilibration with the varying humidity of the air. But the effects of floral visitation by insects on nectar amino acids were also important, both in open flowers and in those with long corollas and more enclosed nectar. Visitors could add amino acids to nectar by direct contact, by salivation, by damaging the neighbouring tissues causing cell leakage, and by dislodging pollen into the nectar; the importance of each of these effects varied according to corolla morphology and the spectrum of visitors.     

Adaptations to a diet of nectar and pollen in the marsupial Tarsipes rostratus (Marsupialia: Tarsipedidae)

The mouse-sized marsupial Tarsipes rostratus , endemic to south-western Australia, feeds almost exclusively on nectar and pollen. Its tongue has long filiform papillae at the tip and shorter compound papillae over much of the upper surface. These collect nectar and pollen when the long tongue, stiffened by a keratinized keel, is protruded into flowers or over pollen presenters. Pollen is scraped from the papillae by a series of combs on the roof of the mouth. A large diverticulum, off the main chamber of the stomach, may store nectar in times of surplus. Pollen is not digested in the stomach but during passage down the simple intestine, which does not have a caecum. In captive animals, pollen passed through the gut in about six hours and the percentage of grains voided which had lost their contents was related to time spent in the gut. The digestion process remains unresolved but probably takes place through the apertures in the shells of pollen grains. Tarsipes ingests large numbers of pollen grains whose contents probably provide necessary nutrients absent from nectar.     

A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore

Host plant chemical composition critically shapes the performance of insect herbivores feeding on them. Some insects have become specialized on plant secondary metabolites, and even use them to their own advantage such as defense against predators. However, infection by plant pathogens can seriously alter the interaction between herbivores and their host plants. We tested whether the effects of the plant secondary metabolites, iridoid glycosides (IGs), on the performance and immune response of an insect herbivore are modulated by a plant pathogen. We used the IG‐specialized Glanville fritillary butterfly Melitaea cinxia, its host plant Plantago lanceolata, and the naturally occurring plant pathogen, powdery mildew Podosphaera plantaginis, as model system. Pre‐diapause larvae were fed on P. lanceolata host plants selected to contain either high or low IGs, in the presence or absence of powdery mildew. Larval performance was measured by growth rate, survival until diapause, and by investment in immunity. We assessed immunity after a bacterial challenge in terms of phenoloxidase (PO) activity and the expression of seven pre‐selected insect immune genes (qPCR). We found that the beneficial effects of constitutive leaf IGs, that improved larval growth, were significantly reduced by mildew infection. Moreover, mildew presence downregulated one component of larval immune response (PO activity), suggesting a physiological cost of investment in immunity under suboptimal conditions. Yet, feeding on mildew‐infected leaves caused an upregulation of two immune genes, lysozyme and prophenoloxidase. Our findings indicate that a plant pathogen can significantly modulate the effects of secondary metabolites on the growth of an insect herbivore. Furthermore, we show that a plant pathogen can induce contrasting effects on insect immune function. We suspect that the activation of the immune system toward a plant pathogen infection may be maladaptive, but the actual infectivity on the larvae should be tested.     

Algal metallothioneins: secondary metabolites and proteins

Metallothioneins, MT's, are low-molecular-weight, cysteine-rich, polypeptides that complex ‘soft’ metal ions in thiol clusters. They are structurally diverse. Some MT's are gene products, while others are secondary metabolites. Two of the three classes of MT have been identified in algae. Eukaryotic algae possess the secondary metabolites referred to as class III MT. There is no unequivocal evidence that MT genes occur in eukaryotic algae. However, the products of MT genes have been identified in cyanobacteria. These genes and their metal regulatory elements remain to be isolated and characterized. MT's have attracted interest from researchers involved in a wide range of disciplines including bioinorganic chemistry, biochemistry, molecular biology, physiology, toxicology, environmental science and medicine. Although, the precise physiological roles of these polypeptides remain undefined, a large number of functions have been speculated. These molecules chelate toxic trace metals, such as Cd, thereby reducing the concentration of cytotoxic, free-metal ions. Furthermore, some MT's are believed to be involved in zinc and copper homoeostasis. Future studies should reveal whether or not some of the diversity of MT structure reflects a diversity of function.     

Colour learning when foraging for nectar and pollen: bees learn two colours at once

Bees are model organisms for the study of learning and memory, yet nearly all such research to date has used a single reward, nectar. Many bees collect both nectar (carbohydrates) and pollen (protein) on a single foraging bout, sometimes from different plant species. We tested whether individual bumblebees could learn colour associations with nectar and pollen rewards simultaneously in a foraging scenario where one floral type offered only nectar and the other only pollen. We found that bees readily learned multiple reward–colour associations, and when presented with novel floral targets generalized to colours similar to those trained for each reward type. These results expand the ecological significance of work on bee learning and raise new questions regarding the cognitive ecology of pollination.     

The agonist paradox: agonists and antagonists of acetylcholine receptors and opioid receptors

In contrast to antagonists, agonists tend to induce considerable conformational changes in their receptors, resulting in opening of ion channels, either directly or via secondary messengers. These conformational transformations require great energy expenses. However, the experimentally determined free energies of complexation between agonists and receptors are often relatively smaller than those for the corresponding antagonists. To rationalize this so-called 'agonist paradox', which has not been clarified in the literature, we have developed an alternative model. Our model may help to discriminate between agonists and antagonists of the acetylcholine (ACh) and mu-opioid receptors. For this purpose, a series of ligands (1-18) have been analyzed both in structural terms and with respect to complexation geometry within the anionic binding sites of these two receptor types.     

Impact of enhanced ultraviolet-B radiation on flower, pollen, and nectar production

Intensified ultraviolet-B radiation or UV-B (wavelengths between 280 and 320 nm) can delay flowering and diminish lifetime flower production in a few plants. Here we studied the effects of enhanced UV-B on floral traits crucial to pollination and pollinator reproduction. We observed simultaneous flowering responses of a new crop plant, Limnanthes alba (Limnathaceae), and a wildflower, Phacelia campanularia (Hydrophyllaceae), to five lifetime UV-B dosages ranging between 2.74 and 15.93 kJ·m·d. Floral traits known to link plant pollination with bee host preference, host fidelity and larval development were measured. Intensified UV-B had no overall effect on nectar and pollen production of L. alba and P. campanularia flowers. A quadratic relationship between UV-B and nectar sugar production occurred in P. campanularia and showed that even subambient UV-B dosages can be deleterious for a floral trait. Other floral responses to UV-B were more dramatic and idiosyncratic. As UV-B dosage increased, L. alba plants were less likely to flower, but suffered no delays in flowering or reductions to lifetime flower production for those that did flower. Conversely, an equal proportion of P. campanularia plants flowered under all UV-B treatments, but these same plants experienced delayed onset to bloom and produced fewer flowers at greater UV-B intensities. Therefore, intensified UV-B elicits idiosyncratic responses in flowering phenology and flower production from these two annual plants. Diurnal patterns in nectar and pollen production strongly coincided with fluctuating humidity and only weakly with UV-B dosage. Overall, our results indicated that intensified UV-B can alter some flowering traits that impinge upon plant competition for pollinator services, as well as plant and pollinator reproductive success.     

The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio

It has been suggested that the absence of floral rewards in many orchid species causes pollinators to probe fewer flowers on a plant, and thus reduces geitonogamy, i.e. self-pollination between flowers, which may result in inbreeding depression and reduced pollen export. We examined the effects of nectar addition on pollinator visitation and pollen transfer by tracking the fate of colour-labelled pollen in Anacamptis morio, a non-rewarding orchid species pollinated primarily by queen bumble-bees. Addition of nectar to spurs of A. morio significantly increased the number of flowers probed by bumble-bees, the time spent on an inflorescence, pollinarium removal and the proportion of removed pollen involved in self-pollination through geitonogamy, but did not affect pollen carryover (the fraction of a pollinarium carried over from one flower to the next). Only visits that exceeded 18 s resulted in geitonogamy, as this is the time taken for removed pollinaria to bend into a position to strike the stigma. A mutation for nectar production in A. morio would result in an initial 3.8-fold increase in pollinarium removal per visit, but also increase geitonogamous self-pollination from less than 10% of pollen depositions to ca. 40%. Greater efficiency of pollen export will favour deceptive plants when pollinators are relatively common and most pollinaria are removed from flowers or when inbreeding depression is severe. These findings provide empirical support both for Darwin's contention that pollinarium bending is an anti-selfing mechanism in orchids and for the idea that floral deception serves to maximize the efficiency of pollen export.