The roots of most land plants are colonised by mycorrhizal fungi that provide mineral nutrients in exchange for carbon. Here, we show that mycorrhizal mycelia can also act as a conduit for signalling between plants, acting as an early warning system for herbivore attack. Insect herbivory causes systemic changes in the production of plant volatiles, particularly methyl salicylate, making bean plants, Vicia faba, repellent to aphids but attractive to aphid enemies such as parasitoids. We demonstrate that these effects can also occur in aphid-free plants but only when they are connected to aphid-infested plants via a common mycorrhizal mycelial network. This underground messaging system allows neighbouring plants to invoke herbivore defences before attack. Our findings demonstrate that common mycorrhizal mycelial networks can determine the outcome of multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbivores and their natural enemies.
Natural enemies respond to herbivore-induced plant volatiles (HIPVs), but an often overlooked aspect is that there may be genotypic variation in these 'indirect' plant defence traits within plant species. We found that egg deposition by stemborer moths (Chilo partellus) on maize landrace varieties caused emission of HIPVs that attract parasitic wasps. Notably, however, the oviposition-induced release of parasitoid attractants was completely absent in commercial hybrid maize varieties. In the landraces, not only were egg parasitoids (Trichogramma bournieri) attracted but also larval parasitoids (Cotesia sesamiae). This implies a sophisticated defence strategy whereby parasitoids are recruited in anticipation of egg hatching. The effect was systemic and caused by an elicitor, which could be extracted from egg materials associated with attachment to leaves. Our findings suggest that indirect plant defence traits may have become lost during crop breeding and could be valuable in new resistance breeding for sustainable agriculture.
Insect pheromones offer potential for managing pests of crop plants. Volatility and instability are problems for deployment in agriculture but could be solved by expressing genes for the biosynthesis of pheromones in the crop plants. This has now been achieved by genetically engineering a hexaploid variety of wheat to release (E)-β-farnesene (Eβf), the alarm pheromone for many pest aphids, using a synthetic gene based on a sequence from peppermint with a plastid targeting amino acid sequence, with or without a gene for biosynthesis of the precursor farnesyl diphosphate. Pure Eβf was produced in stably transformed wheat lines with no other detectable phenotype but requiring targeting of the gene produced to the plastid. In laboratory behavioural assays, three species of cereal aphids were repelled and foraging was increased for a parasitic natural enemy. Although these studies show considerable potential for aphid control, field trials employing the single and double constructs showed no reduction in aphids or increase in parasitism. Insect numbers were low and climatic conditions erratic suggesting the need for further trials or a closer imitation, in the plant, of alarm pheromone release.
Malaria parasites () can change the attractiveness of their vertebrate hosts to vectors, leading to a greater number of vector-host contacts and increased transmission. Indeed, naturally-infected children have been shown to attract more mosquitoes than parasite-free children. Here, we demonstrate -induced increases in the attractiveness of skin odor in Kenyan children and reveal quantitative differences in the production of specific odor components in infected vs. parasite-free individuals. We found the aldehydes heptanal, octanal, and nonanal to be produced in greater amounts by infected individuals and detected by mosquito antennae. In behavioral experiments, we demonstrated that these, and other,-induced aldehydes enhanced the attractiveness of a synthetic odor blend mimicking "healthy" human odor. Heptanal alone increased the attractiveness of "parasite-free" natural human odor. Should the increased production of these aldehydes by -infected humans lead to increased mosquito biting in a natural setting, this would likely affect the transmission of malaria.
Plant volatiles play important roles in attraction of certain pollinators and in host location by herbivorous insects. Virus infection induces changes in plant volatile emission profiles, and this can make plants more attractive to insect herbivores, such as aphids, that act as viral vectors. However, it is unknown if virus-induced alterations in volatile production affect plant-pollinator interactions. We found that volatiles emitted by cucumber mosaic virus (CMV)-infected tomato (Solanum lycopersicum) and Arabidopsis thaliana plants altered the foraging behaviour of bumblebees (Bombus terrestris). Virus-induced quantitative and qualitative changes in blends of volatile organic compounds emitted by tomato plants were identified by gas chromatography-coupled mass spectrometry. Experiments with a CMV mutant unable to express the 2b RNA silencing suppressor protein and with Arabidopsis silencing mutants implicate microRNAs in regulating emission of pollinator-perceivable volatiles. In tomato, CMV infection made plants emit volatiles attractive to bumblebees. Bumblebees pollinate tomato by ‘buzzing’ (sonicating) the flowers, which releases pollen and enhances self-fertilization and seed production as well as pollen export. Without buzz-pollination, CMV infection decreased seed yield, but when flowers of mock-inoculated and CMV-infected plants were buzz-pollinated, the increased seed yield for CMV-infected plants was similar to that for mock-inoculated plants. Increased pollinator preference can potentially increase plant reproductive success in two ways: i) as female parents, by increasing the probability that ovules are fertilized; ii) as male parents, by increasing pollen export. Mathematical modeling suggested that over a wide range of conditions in the wild, these increases to the number of offspring of infected susceptible plants resulting from increased pollinator preference could outweigh underlying strong selection pressures favoring pathogen resistance, allowing genes for disease susceptibility to persist in plant populations. We speculate that enhanced pollinator service for infected individuals in wild plant populations might provide mutual benefits to the virus and its susceptible hosts.
The boll weevil, Anthonomus grandis, has been monitored through deployment of traps baited with aggregation pheromone components. However, field studies have shown that the number of insects caught in these traps is significantly reduced during cotton squaring, suggesting that volatiles produced by plants at this phenological stage may be involved in attraction. Here, we evaluated the chemical profile of volatile organic compounds (VOCs) emitted by undamaged or damaged cotton plants at different phenological stages, under different infestation conditions, and determined the attractiveness of these VOCs to adults of A. grandis. In addition, we investigated whether or not VOCs released by cotton plants enhanced the attractiveness of the aggregation pheromone emitted by male boll weevils. Behavioral responses of A. grandis to VOCs from conspecific-damaged, heterospecific-damaged (Spodoptera frugiperda and Euschistus heros) and undamaged cotton plants, at different phenological stages, were assessed in Y-tube olfactometers. The results showed that volatiles emitted from reproductive cotton plants damaged by conspecifics were attractive to adults boll weevils, whereas volatiles induced by heterospecific herbivores were not as attractive. Additionally, addition of boll weevil-induced volatiles from reproductive cotton plants to aggregation pheromone gave increased attraction, relative to the pheromone alone. The VOC profiles of undamaged and mechanically damaged cotton plants, in both phenological stages, were not different. Chemical analysis showed that cotton plants produced qualitatively similar volatile profiles regardless of damage type, but the quantities produced differed according to the plant's phenological stage and the herbivore species. Notably, vegetative cotton plants released higher amounts of VOCs compared to reproductive plants. At both stages, the highest rate of VOC release was observed in A. grandis-damaged plants. Results show that A. grandis uses conspecific herbivore-induced volatiles in host location, and that homoterpene compounds, such as (E)-4,8-dimethylnona-1,3,7-triene and (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene and the monoterpene (E)-ocimene, may be involved in preference for host plants at the reproductive stage.
Malaria parasites are thought to influence mosquito attraction to human hosts, a phenomenon that may enhance parasite transmission. This is likely mediated by alterations in host odour because of its importance in mosquito host-searching behaviour. Here, we report that the human skin odour profile is affected by malaria infection. We compared the chemical composition and attractiveness to Anopheles coluzzii mosquitoes of skin odours from participants that were infected by Controlled Human Malaria Infection with Plasmodium falciparum. Skin odour composition differed between parasitologically negative and positive samples, with positive samples collected on average two days after parasites emerged from the liver into the blood, being associated with low densities of asexual parasites and the absence of gametocytes. We found a significant reduction in mosquito attraction to skin odour during infection for one experiment, but not in a second experiment, possibly due to differences in parasite strain. However, it does raise the possibility that infection can affect mosquito behaviour. Indeed, several volatile compounds were identified that can influence mosquito behaviour, including 2- and 3-methylbutanal, 3-hydroxy-2-butanone, and 6-methyl-5-hepten-2-one. To better understand the impact of our findings on Plasmodium transmission, controlled studies are needed in participants with gametocytes and higher parasite densities.
bWe hypothesized that interactions between fusarium head blight-causing pathogens and herbivores are likely to occur because they share wheat as a host plant. Our aim was to investigate the interactions between the grain aphid, Sitobion avenae, and Fusarium graminearum on wheat ears and the role that host volatile chemicals play in mediating interactions. Wheat ears were treated with aphids and F. graminearum inoculum, together or separately, and disease progress was monitored by visual assessment and by quantification of pathogen DNA and mycotoxins. Plants exposed to both aphids and F. graminearum inoculum showed accelerated disease progression, with a 2-fold increase in disease severity and 5-fold increase in mycotoxin accumulation over those of plants treated only with F. graminearum. Furthermore, the longer the period of aphid colonization of the host prior to inoculation with F. graminearum, the greater the amount of pathogen DNA that accumulated. Headspace samples of plant volatiles were collected for use in aphid olfactometer assays and were analyzed by gas chromatography-mass spectrometry (GC-MS) and GC-coupled electroantennography. Disease-induced plant volatiles were repellent to aphids, and 2-pentadecanone was the key semiochemical underpinning the repellent effect. We measured aphid survival and fecundity on infected wheat ears and found that both were markedly reduced on infected ears. Thus, interactions between F. graminearum and grain aphids on wheat ears benefit the pathogen at the expense of the pest. Our findings have important consequences for disease epidemiology, because we show increased spread and development of host disease, together with greater disease severity and greater accumulation of pathogen DNA and mycotoxin, when aphids are present. P lant interactions with pathogens or insects are usually studied in isolation, even though plants are exposed to both in the field. It is likely that organisms that share the same host plant can alter its condition and thereby interact with each other. Although Fusarium pathogens and grain aphids cause substantial damage to wheat and coincide, little is known about interactions between these species.Fusarium head blight (FHB) is a disease of small grain cereals that occurs globally and is caused by a complex of species from the genera Fusarium and Microdochium (1, 2). The most aggressive species causing FHB is Fusarium graminearum, a potent producer of the mycotoxin deoxynivalenol (DON), which is harmful to human and animal health if consumed (3). European legislation has set the acceptable limit of DON in grain marketed for human consumption at 1,250 g kg Ϫ1 (4) in unprocessed cereals. Consequently, FHB epidemics result in large economic losses from the combined effects of reductions in yield, increased mycotoxin contamination, and reduced quality and marketability of the crop (5).In the spring, ascospores and/or conidia of Fusarium graminearum are released from crop residues and are spread by wind or rainsplash. Wheat is most susceptible to FHB du...
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