Plant Proteinase inhibitors: A defense against herbivorous insects?

Using the tomato plant, Lycopersicon esculentum L., and the beet armyworm, Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), we have demonstrated that insect herbivory induces a rapid decline in plant quality. This decline in plant quality manifests itself by a highly significant reduction in rate of larval growth on a medium containing foliage from insect-damaged as opposed to undamaged tomato plants. The induction of tomato proteinase inhibitors, as a result of larval feeding, is invoked as a factor that systemically reduces leaf quality.

---

Zusammenfassung Eine zentrale Theorie in der Erforschung von Insekten-Wirtspflanzen-Wechselbeziehungen ist, dass sich bestimmte natürlich vorkommende Pflanzeninhaltsstoffe in Pflanzen zur Abwehr herbivorer Insekten und anderer Parasiten entwickelt haben. Zur Zeit herrschende Überlegungen beinhalten auch das Konzept, dass herbivore Insekten das Potential besitzen, Veränderungen in der Abwehrund/oder Nahrungsqualität von Wirtspflanzen hervorzurufen, die den herbivoren Insekten schaden. Gegenwärtig is nur wenig über die Ursachen dieser von Insekten induzierten Veränderungen der Wirtspflanzenqualität bekannt. Jedoch werden häufig unterschiedliche Gehalte der Pflanzen an Phenolderivaten, Protein und/oder Proteinaseinhibitoren mit den Abwehrmechanismen in Zusammenhang gebracht. Diese Arbeit untersucht das Potential von Pflanzenproteinaseinhibitoren, als induzierbare Abwehr gegen herbivore Noctuidenlarven zu wirken.Tomatenpflanzen enthalten Proteinaseinhibitoren (PIs), die durch Verletzen der Pflanze induziert werden. Es besteht die Hypothese, dass diese Synthese von PIs einen Abwehrmechanismus gegen blattfressende Insekten darstellt. Diese Hypothese ist niemals angemessen in planta getestet worden und wird von uns anhand von Spodoptera exigua und Tomatenpflanzen, Lycopersicon esculentum, getestet.Wieterhin sollte festgestellt werden, ob eine Beziehung zwischen der PI-Konzentration im Blatt und dem Wachstum von Blattmaterial fressenden Larven besteht. Anstelle lebender Pflanzen wurde dazu eine feste, Blattmaterial enthaltende Diät (15% gefriergetrocknetes Blattmaterial angemischt in Agarlösung und Sorbinsäure) benutzt, was die Verwending einer unverletzten Kontrolle ermöglichte. Diese künstliche Diät wurde S. exigua angeboten. Die Ergebnisse des Fütterungsversuches (Fig. 2) zeigen, dass eine signifikante inverse Beziehung (r²=0.81, p=0.05) zwischen der PI-Konzentration im Blattgewebe und den mittleren Gewichten von Larven von S. exigua besteht. Nicht dargestellt ist die nicht signifikante Korrelation zwischen mittlerem Gewicht der Larven und den Gehalten an Blattprotein (r²=0.47, p>0.25) und Phenolderivaten (r²=0.50, p=0.25).Diese Ergebnisse veranlassen uns zu dem Rückschluss, dass Tomatenproteinaseinhibitoren als systemisch induzierbare antibiotische chemische Abwehr gegen herbivore Insekten wie Noctuidenlarven anzusehen sind, und dass PIs einen Faktor darstellen, der zur systemischen Reduktion der Blattqualität von Tomaten führt.

     

Does attraction to frugivores or defense against pathogens shape fruit pulp composition?

Fruit traits evolve in response to an evolutionary triad between plants, seed dispersers, and antagonists that consume fruits but do not disperse seeds. The defense trade-off hypothesis predicts that the composition of nutrients and of secondary compounds in fruit pulp is shaped by a trade-off between defense against antagonists and attraction to seed dispersers. The removal rate model of this hypothesis predicts a negative relationship between nutrients and secondary compounds, whereas the toxin-titration model predicts a positive relationship. To test these alternative models, we evaluated whether the contents of nutrients and secondary compounds can be used to predict fruit removal by mutualists and pathogens in 14 bird-dispersed plants on a subtropical island in São Paulo state, southeastern Brazil. We selected eight to ten individuals of each species and prevented fruit removal by covering four branches with a net and left fruits on four other branches available to both, vertebrate fruit consumers and pathogens. The persistence of ripe fruits was drastically different among species for bagged and open fruits, and all fruit species persisted longer when protected against seed dispersers. We found that those fruits that are quickly removed by vertebrates are nutrient-rich, but although the attack rate of pathogens is also high, these fruits have low contents of quantitative defenses such as tannins and phenols. Thus, we suggest that the fruit removal rate by seed dispersers is the primary factor selecting the levels of fruit defense. Likewise, nutrient-poor fruits have low removal of seed dispersers and low probability of attack by pathogens. These species retain ripe fruits in an intact condition for a prolonged period because they are highly defended by secondary compounds, which reduce overall attractiveness. However, this strategy might be advantageous for plants that depend on rare or unreliable dispersers.     

Can plants use an entomopathogenic virus as a defense against herbivores?

It is by now well established that plants use various strategies to defend themselves against herbivores. Besides conventional weapons such as spines and stinging hairs and sophisticated chemical defenses, plants can also involve the enemies of the herbivores in their defense. It has been suggested that plants could even use entomopathogens as part of their defense strategies. In this paper, we show that Brassica oleraceae plants that are attacked by Myzus persicae aphids infected with an entomopathogenic parvovirus (M. persicae densovirus) transport the virus through the phloem locally and systematically. Moreover, healthy aphids that fed on the same leaf, but separated from infected aphids were infected via the plant. Hence, this is proof of the principle that plants can be vectors of an insect virus and can possibly use this virus as a defense against herbivores.     

Plant allelochemical interference or soil chemical ecology?

While allelopathy has been defined as plant-plant chemical interference, there has been much confusion about what the concept encompasses and how important it is in nature. We distinguish between (1) direct plant-plant interference mediated by allelochemicals, and (2) the effects of secondary compounds released by plants on abiotic and biotic soil processes that affect other plants.It very difficult to demonstrate direct effects of chemicals released by a plant on nearby plants. Although soil ecology-mediated effects of secondary plant compounds do not fit the classical concept of allelopathy, we find support in the literature for the hypothesis that the most important effects of compounds released into the soil environment by plants on other plants occur through such indirect effects. The emphasis on, and skepticism of, direct plant-plant allelopathic interference has led some researchers to demand unreasonably high standards of evidence for establishing even the existence of allelopathic interactions, standards that are not demanded for other plant-plant interactions such as resource competition. While the complete elucidation of the mechanisms by which allelochemicals function in the field is many years away, such elucidation is not necessary to establish the existence of allelopathic interactions.We propose that most of the phenomena broadly referred to as allelopathic interference are better conceptualized and investigated in terms of soil chemical ecology. Even when direct plant-plant allelochemical interference occur, the levels of allelochemicals in the environment and their effects on plants are heavily influenced by abiotic and biotic components of the soil ecosystem. Putting allelopathy in the context of soil ecology can further research and reduce some of the less fruitful controversy surrounding the phenomenon.     

Plant fructan exohydrolases: a role in signaling and defense?

Fructans are fructose oligomers and polymers synthesized by a small number of plant and bacterial species and mainly function as reserve carbohydrates. The terminal fructosyl-fructose linkages can be degraded by fructan exohydrolases (FEHs), occurring in bacteria, fungi and fructan plants. Unexpectedly, it was found that FEHs also occur in non-fructan plants such as Beta vulgaris and Arabidopsis thaliana that apparently lack endogenous fructan substrates. FEHs might have defense-related roles acting on bacterial fructan-containing slimes or might act on minute (up to now undetected) amounts of fructans acting as signals in plants.     

Gamma-aminobutyrate: defense against invertebrate pests?

Gamma-aminobutyrate (GABA) is a ubiquitous four-carbon, non-protein amino acid. In plants, stress-induced GABA accumulation is well documented. However, the role(s) of GABA accumulation is contentious. In this Opinion article, we argue that wounding due to herbivory and crawling by insect larvae causes rapid GABA accumulation via the disruption of cellular compartmentation and the release of the acidic vacuolar contents to the cytosol. The activity of glutamate decarboxylase, the cytosolic enzyme responsible for GABA synthesis, has an acidic pH optimum. Subsequent GABA ingestion has a plant defense function by directly acting on GABA-regulated invertebrate neuromuscular junctions. Plants with an enhanced GABA-producing capacity reduce herbivory by invertebrate pests. These findings suggest that GABA accumulation is a rapidly deployed, local resistance mechanism that constitutes a first line of defense in deterring herbivory.     

BVOCs: plant defense against climate warming?

Plants emit a substantial amount of biogenic volatile organic compounds (BVOCs) into the atmosphere. These BVOCs represent a large carbon loss and can be up to approximately 10% of that fixed by photosynthesis under stressful conditions and up to 100gCm(-2) per year in some tropical ecosystems. Among a variety of proven and unproven BVOC functions in plants and roles in atmospheric processes, recent data intriguingly link emission of these compounds to climate. Ongoing research demonstrates that BVOCs could protect plants against high temperatures. BVOC emissions are probably increasing with warming and with other factors associated to global change, including changes in land cover. These increases in BVOC emissions could contribute in a significant way (via negative and positive feedback) to the complex processes associated with global warming.     

Resveratrol and its analogs: defense against cancer, coronary disease and neurodegenerative maladies or just a fad?

Resveratrol (3,5,4'-trihydroxy-trans-stilbene; RV), a dietary constituent found in grapes and wine, exerts a wide variety of pharmacological activities. Because the grape skins are not fermented in the production process of white wines, only red wines contain considerable amounts of this compound. RV is metabolized into sulfated and glucuronidated forms within approximately 15min of entering the bloodstream, and moderate consumption of red wine results in serum levels of RV that barely reach the micromolar concentrations. In contrast, its metabolites, which may be the active principle, circulate in serum for up to 9h. RV has been identified as an effective candidate for cancer chemoprevention due its ability to block each step in the carcinogenesis process by inhibiting several molecular targets such as kinases, cyclooxygenases, ribonucleotide reductase, and DNA polymerases. In addition, RV protects the cardiovascular system by a large number of mechanisms, including defense against ischemic-reperfusion injury, promotion of vasorelaxation, protection and maintenance of intact endothelium, anti-atherosclerotic properties, inhibition of low-density lipoprotein oxidation, and suppression of platelet aggregation, thereby strongly supporting its role in the prevention of coronary disease. Promising data within the use of RV have also been obtained regarding progressive neurodegenerative maladies such as Alzheimer's, Huntington's, and Parkinson's diseases. Because neurotoxicity is often related to mitochondrial dysfunction and may be ameliorated through the inclusion of metabolic modifiers and/or antioxidants, RV may provide an alternative (and early) intervention approach that could prevent further damage. RV induces a multitude of effects that depend on the cell type (e.g., NF-kappaB modulation in cancer cells vs. neural cells), cellular condition (normal, stressed, or malignant), and concentration (proliferative vs. growth arrest), and it can have opposing activities. RV affects whole pathways and sets of intracellular events rather than a single enzyme and, therefore, may be an effective therapy to restore homoestasis. Nonetheless, the question of whether RV or its metabolites can accumulate to bioactive levels in target organs remains to be addressed.     

Will chemical defenses become more effective against specialist herbivores under elevated CO2?

Elevated atmospheric CO₂ is known to affect plant–insect herbivore interactions. Elevated CO₂ causes leaf nitrogen to decrease, the ostensible cause of herbivore compensatory feeding. CO₂ may also affect herbivore consumption by altering chemical defenses via changes in plant hormones. We considered the effects of elevated CO₂, in conjunction with soil fertility and damage (simulated herbivory), on glucosinolate concentrations of mustard (Brassica nigra) and collard (B. oleracea var. acephala) and the effects of leaf nitrogen and glucosinolate groups on specialist Pieris rapae consumption. Elevated CO₂ affected B. oleracea but not B. nigra glucosinolates; responses to soil fertility and damage were also species‐specific. Soil fertility and damage also affected B. oleracea glucosinolates differently under elevated CO₂. Glucosinolates did not affect P. rapae consumption at either CO₂ concentration in B. nigra, but had CO₂‐specific effects on consumption in B. oleracea. At ambient CO₂, leaf nitrogen had strong effects on glucosinolate concentrations and P. rapae consumption but only gluconasturtiin was a feeding stimulant. At elevated CO₂, direct effects of leaf nitrogen were weaker, but glucosinolates had stronger effects on consumption. Gluconasturtiin and aliphatic glucosinolates were feeding stimulants and indole glucosinolates were feeding deterrents. These results do not support the compensatory feeding hypothesis as the sole driver of changes in P. rapae consumption under elevated CO₂. Support for hormone‐mediated CO₂ response (HMCR) was mixed; it explained few treatment effects on constitutive or induced glucosinolates, but did explain patterns in SEMs. Further, the novel feeding deterrent effect of indole glucosinolates under elevated CO₂ in B. oleracae underscores the importance of defensive chemistry in CO₂ response. We speculate that P. rapae indole glucosinolate detoxification mechanisms may have been overwhelmed under elevated CO₂ forcing slowed consumption. Specialists may have to contend with hosts with poorer nutritional quality and more effective chemical defenses under elevated CO₂.     

Facilitation of tree saplings by nurse plants: Microhabitat amelioration or protection against herbivores?

Question: Positive interactions are predicted to be common in communities developing under high physical stress or high herbivory pressure due to neighbour amelioration of limiting physical and consumer stresses, respectively. However, when both stress sources meet in the same community, the relative importance of the two facilitation mechanisms is poorly understood. We ask: What is the relative importance of abiotic vs. biotic mechanisms of facilitation of tree saplings by shrubs in Mediterranean mountain forests? Location: Sierra Nevada, SE Spain (1800–1850 m a.s.l.) Methods: Saplings of four tree taxa (Acer opalus ssp. grana‐tense, Quercus ilex, Pinus nigra ssp. salzmanii and P. sylvestris var. nevadensis) were planted following a 2 × 2 factorial design: two levels of herbivory (control and ungulate exclusion) and two microhabitats (under shrubs and in open areas). Sapling survival and growth were monitored for five years. Results: Shrubs had positive effects on sapling survival both in control and ungulate excluded plots. This effect was species‐specific, with shrubs increasing the survival of Acer opalus and Quercus ilex three and twofold, respectively, but having a minor effect on the Pinus species. Herbivory damage was also species‐specific, being much higher for Acer opalus than for any other species. Shrubs did not protect saplings of any species against ungulates. Thus, all Acer saplings (the most damaged species) suffered herbivory outside the exclosures, which largely reduced sapling height. Conclusions: Protection from abiotic stress (summer drought and winter frost) was much more relevant than protection from biotic stress (herbivory). However, we propose that the final balance between the two mechanisms can be expected to vary strongly between sites, depending on the relative magnitude of the different sources of stress and the intrinsic traits (e.g. palatability) of the species interacting.     

The herbivores’ dilemma: trade-offs between nutrition and parasitism in foraging decisions

An experiment was carried out using a trade-off framework to determine the rules of sward selection, in relation to gastrointestinal parasite dispersion, used by mammalian herbivores, and the effect of level of feeding motivation and parasitic status on these rules. Twenty-four sheep divided into four animal treatment groups resulting from two levels of feeding motivation (high and moderate) and two parasitic states (parasitised with Ostertagia circumcincta and non-parasitised) were presented with pairs of experimental swards which varied in N content (high and low), sward height (tall and short) and level of contamination with faeces and thus parasites (contaminated and non-contaminated). The selection for tall swards outweighed both the selection for N-rich swards and the avoidance of faecal contaminated swards. The selection for N-rich swards could not completely overcome faecal avoidance. Parasitism in animals with a moderate feeding motivation reduced their bite rates and grazing depths, thereby probably reducing the rate of ingestion of parasitic larvae. In contrast, highly feeding-motivated animals (including those parasitised) increased their bite rates and grazing depths, thereby increasing the rate of ingestion of parasites. The inclusion of parasite distributions, both in the environment and within herbivore host populations, is likely to advance optimal foraging theory by enhancing its predictive power. Received: 30 November 1999 / Accepted: 14 February 2000     

Secreted ferritin: Mosquito defense against iron overload?

The yellow fever mosquito, Aedes aegypti, must blood feed in order to complete her life cycle. The blood meal provides a high level of iron that is required for egg development. We are interested in developing control strategies that interfere with this process. We show that A. aegypti larval cells synthesize and secrete ferritin in response to iron exposure. Cytoplasmic ferritin is maximal at low levels of iron, consists of both the light chain (LCH) and heavy chain (HCH) subunits and reflects cytoplasmic iron levels. Secreted ferritin increases in direct linear relationship to iron dose and consists primarily of HCH subunits. Although the messages for both subunits increase with iron treatment, our data indicate that mosquito HCH synthesis could be partially controlled at the translational level as well. Importantly, we show that exposure of mosquito cells to iron at low concentrations increases cytoplasmic iron, while higher iron levels results in a decline in cytoplasmic iron levels indicating that excess iron is removed from mosquito cells. Our work indicates that HCH synthesis and ferritin secretion are key factors in the response of mosquito cells to iron exposure and could be the primary mechanisms that allow these insects to defend against an intracellular iron overload.     

Territorial behavior in Southeast Asian langurs: Resource defense or mate defense?

Between-group antagonism or territoriality in primates may serve two different but compatible functions: resource defense or mate defense. Females are expected to be involved more strongly in the first, males in the second. The resource defense hypothesis predicts that home range overlap should decrease as defensibility and population density increase, and that females should be involved in hostile between-group interactions. The mate defense hypothesis predicts that between-group relations should be hostile and that males should take the primary role in antagonistic encounters. In a comparative study of 12 populations of 6 Presbytis species in Southeast Asia, we found support for the mate defense hypothesis; only males produce loud calls, between-group antagonism is entirely a male affair, and neither defensibility nor population density determine spatial exclusivity or the level of antagonism. We discuss the differences between our findings and traditional interpretations of territorial behavior.     

Worm therapy: for or against?

This article succinctly reviews the weight of evidence supporting worm therapy, and asks the question whether the evidence is sufficient to support the use of parasitic worms as investigational medicinal products.     

Ant–plant interactions: the importance of extrafloral nectaries versus hemipteran honeydew on plant defense against herbivores

The two most important ant–plant attractions are extrafloral nectaries (EFNs) and hemipteran honeydew. In both cases, ants may offer an effective protection against natural enemies of plants, in exchange for its sugar-rich exudates. The aim of this paper was to compare the efficiency of ant protection between plants with EFNs and with hemipteran honeydew. The study was carried out in the Amazonian Rain Forest Reserve at km 41 (02º 24′S, 59º 44′W), located 80 km from Manaus. We recorded 24 ant species in 25 plants species in the forest understory along two line transects of 5 km. The efficiency of ants in protecting plants was measured by an experiment of prey removal using isopteran workers. It was found that ants are more effective and faster in attacking termites when using honeydew rather than EFNs, probably due to the larger resource monopolization. This study further underlines the importance of experimental studies to elucidate the ecological and evolutionary importance of EFNs and honeydew in ant–plant defense against herbivores.     

Bacteriophage biocontrol of plant pathogens: fact or fiction?

Bacterial resistance due to the misuse of antibiotics has become a global issue and alternative methods are being developed that might decrease the use of antimicrobials in agricultural settings. Bacteriophage therapy represents a novel way to control the growth of plant-based bacterial pathogens. Although this method shows promise, a recent paper by Gill and Abedon has shown that the complex bacteriophage-host interactions in the plant environment must be investigated further.