Reiterative and interruptive signaling in induced plant resistance to chewing insects

Our understanding of induced resistance against herbivores has grown immeasurably during the last several decades. Based upon the emerging literature, we argue that induced resistance represents a continuum of phenotypes that is determined by the plant’s ability to integrate multiple suites of signals of plant and herbivore origin. We present a model that illustrates the range of signals arising from early detection through herbivore feeding, and then through subsequent plant generations.     

Complex interactions between a plant pathogen and insect parasitoid via the shared vector-host: consequences for host plant infection

Plant viruses modify the development of their aphid vectors by inducing physiological changes in the shared host plant. The performance of hymenopterous parasitoids exploiting these aphids can also be modified by the presence of the plant pathogen. We used laboratory and glasshouse microcosms containing beans (Vicia faba) as the host plant to examine the interactions between a plant virus (pea enation mosaic virus; PEMV) and a hymenopterous parasitoid (Aphidius ervi) that share the aphid vector/host Acyrthosiphon pisum. Neither PEMV-infection of V. faba, nor the carriage of PEMV virions by A. pisum, affected the growth or morphology of the aphid, or the oviposition behaviour and development of A. ervi. The presence of developing Aphidius ervi larvae within Acyrthosiphon pisum did not affect the ability of the aphids to transmit PEMV. However, by reducing their longevity, parasitism ultimately decreased the time viruliferous aphids were able to inoculate plants. In terms of virus dispersal, parasitized aphids exhibited more movement around experimental arenas than unparasitized controls, causing a slight increase in the proportion of beans infected with PEMV. Exposure to adult Aphidius ervi caused Acyrthosiphon pisum to rapidly drop off bean plants and disperse to new hosts, resulting in considerably higher plant infection rates (70%) than that seen in control arenas (25%). The results of this investigation demonstrate that when parasitoids are added to a plant-pathogen-vector system, benefits to the host plant due to reduced herbivore infestation must be balanced against the consequences of parasitoid-induced aphid dispersal and a subsequent increase in the level of plant infection.     

A link between virulence and homeostatic responses to hypoxia during infection by the human fungal pathogen Cryptococcus neoformans

Fungal pathogens of humans require molecular oxygen for several essential biochemical reactions, yet virtually nothing is known about how they adapt to the relatively hypoxic environment of infected tissues. We isolated mutants defective in growth under hypoxic conditions, but normal for growth in normoxic conditions, in Cryptococcus neoformans, the most common cause of fungal meningitis. Two regulatory pathways were identified: one homologous to the mammalian sterol-response element binding protein (SREBP) cholesterol biosynthesis regulatory pathway, and the other a two-component-like pathway involving a fungal-specific hybrid histidine kinase family member, Tco1. We show that cleavage of the SREBP precursor homolog Sre1-which is predicted to release its DNA-binding domain from the membrane-occurs in response to hypoxia, and that Sre1 is required for hypoxic induction of genes encoding for oxygen-dependent enzymes involved in ergosterol synthesis. Importantly, mutants in either the SREBP pathway or the Tco1 pathway display defects in their ability to proliferate in host tissues and to cause disease in infected mice, linking for the first time to our knowledge hypoxic adaptation and pathogenesis by a eukaryotic aerobe. SREBP pathway mutants were found to be a hundred times more sensitive than wild-type to fluconazole, a widely used antifungal agent that inhibits ergosterol synthesis, suggesting that inhibitors of SREBP processing could substantially enhance the potency of current therapies.     

Interaction between fungal endophytes and environmental stressors influences plant resistance to insects

Neotyphodium coenophialum, an endophytic fungus that infects shoots of tall fescue (Festuca arundinacea), may protect its host from herbivory through production of alkaloids. Yet, the fungus can also modify plant resource allocation, regrowth dynamics, and drought tolerance, and these changes may also influence herbivores. We tested if N. coenophialum infection interacted with stress (drought or simulated herbivory) to modify plant resistance to insects. We assigned greenhouse plants to one of four treatments: 1) clipping at 3 cm above the soil surface, 2) drought stress during insect bioassays, 3) drought stress prior to insect bioassays, or 4) daily watering. Treatments were crossed with presence or absence of endophyte to give eight treatment combinations, and we assessed the performance of bird cherry‐oat aphid (Rhopalosiphum padi) and fall armyworm (Spodoptera frugiperda) feeding on plants in two separate experiments from each of the eight treatments. Aphids were placed into clip bags on leaf blades and allowed to reproduce parthenogenetically. Plant tissue was fed to third instar fall armyworm caterpillars until they molted into the fifth instar. Developmental time was recorded and larval growth was obtained gravimetrically. We also assessed total protein nitrogen (N) and loline alkaloids in plants.
Total protein N was unaffected by endophyte infection. In contrast, stress influenced total protein N, but its effect varied with endophyte infection. Uninfected plants that were clipped had higher total protein N; this trend was absent in infected plants. Plants in drought stress had lower N, but only if they were infected. Lolines were nearly absent from uninfected plants. In infected plants they tended to be higher in clipped plants. The effect of endophyte infection differed between the two insects: aphid reproduction was reduced by the endophyte, but endophyte infection enhanced caterpillar performance. Both insects were affected by interactions between the endophyte and stress. Aphids were negatively affected by drought stress, but only when feeding on uninfected plants, while caterpillars showed the opposite response, displaying lower performance on drought stressed plants only if they were infected. Aphids reproduced faster on regrowth tissue (following damage by clipping) of uninfected plants, but endophyte infection cancelled this effect. In contrast, performance of caterpillars was not influenced by an interaction between damage and infection. We conclude that N. coenophialum does not provide universal resistance to insects. Endophyte‐mediated resistance varies with insect species and will be a complex function of environmental stress, including drought and prior damage.     

Cross-induction of systemic induced resistance between an insect and a fungal pathogen in Austrian pine over a fertility gradient

Evidence for cross-induction of systemic resistance or susceptibility in plant–fungus–herbivore interactions is mostly derived from herbaceous model systems and not perennial woody plants. Furthermore, the effects of environmental variables such as soil fertility on these tripartite interactions are generally unknown. This study examined cross-induction of systemic resistance in Pinus nigra (Austrian pine) to infection by Sphaeropsis sapinea (a fungal pathogen), or feeding by Neodiprion sertifer (European pine sawfly), by prior induction with either S. sapinea or N. sertifer, over a fertility gradient. In a replicated 3-year study, cross-induction of systemic induced resistance (SIR) was found to be both asymmetric within a single year and variable between years. Prior induction with insect defoliation induced SIR to subsequent fungal challenge in 2006 but not in 2005. In 2005, a fertility-independent negative systemic effect of the fungal infection on herbivore growth was detected while herbivore survival was affected by a significant interaction between induction treatment and fertility level in 2006. Prior infection by the fungus induced SIR against the same fungus in both years regardless of fertility levels. This is the first report of whole-plant SIR against a defoliating insect induced by a fungal pathogen and vice versa, under variable nutrient availability, in a conifer or any other tree. Alieta Eyles and Rodrigo Chorbadjian contributed equally to the paper.     

Rising CO2, secondary plant metabolism,plant-herbivore interactions and litter decomposition

A brief account is given of the ecological significance of quantitatively important secondary plant compounds, mainly those of a phenolic nature, in herbivory and decomposition. Phenolic compounds accumulate to a greater extent in slow-growing species than in fast-growing ones, particularly when soil conditions (nutrients, water) restrict growth. Two hypotheses to explain the increased concentration of phenolics when soil conditions are unfavorable are presented. The first hypothesis (the carbon supply model of secondary plant metabolism) considers the increased levels of non-structural carbohydrates as the major trigger. The second hypothesis (the amino acid diversion model of secondary plant metabolism) states that increased accumulation of phenolics stems from a decreased use of a common precursor (phenylalanine or tyrosine) for protein synthesis. Current experimental evidence, though still fairly limited, supports the second hypothesis, but further testing is required before the first model can be rejected. So far, there is very little evidence for a direct effect of atmospheric CO₂ on the concentration of secondary compounds in higher plants. However, there are likely to be indirect effects, due to a stronger limitation by the nitrogen supply in plants whose growth has been promoted by atmospheric CO₂. It is concluded that it is very likely that phenolic compounds accumulate to a greater extent in plants exposed to elevated CO₂, due to a greater limitation of nutrients, rather than as a direct effect of elevated CO₂.     

Tritrophic interactions between a fungal pathogen,a spider predator,and the blacklegged tick

The blacklegged tick Ixodes scapularis is the primary vector for the bacterium causing Lyme disease in eastern North America and for other medically important pathogens. This species is vulnerable to attack by fungal pathogens and arthropod predators, but the impacts of interactions between biocontrol agents have not been examined. The biocontrol agent Met52^®, containing the entomopathogenic fungus Metarhizium brunneum (=M. anisopliae), controls blacklegged ticks with efficacy comparable to chemical acaricides. The brush‐legged wolf spider Schizocosa ocreata is a predator of I. scapularis that reduces their survival under field conditions. We conducted a field microcosm experiment to assess the compatibility of Met52 and S. ocreata as tick biocontrol agents. We compared the fits of alternative models in predicting survival of unfed (flat) and blood‐fed (engorged) nymphs. We found the strongest support for a model that included negative effects of Met52 and S. ocreata on flat nymph survival. We found evidence for interference between biocontrol agents, with Met52 reducing spider survival, but we did not find a significant interaction effect between the two agents on nymph survival. For engorged nymphs, low recovery rates resulted in low statistical power to detect possible effects of biocontrol agents. We found that nymph questing activity was lower when the spider was active above the leaf litter than when the spider was unobserved. This provides the first evidence that predation cues might affect behavior important for tick fitness and pathogen transmission. This study presents field microcosm evidence that the biopesticide Met52 and spider Schizocosa ocreata each reduced survival of blacklegged ticks Ixodes scapularis. Met52 reduced spider survival. Potential interference between Met52 and the spider should be examined at larger scales, where overlap patterns may differ. Ticks were more likely to quest when the spider was inactive, suggesting the ticks changed their behavior to reduce danger.     

Resistance to a fungal pathogen and host plant specialization in the pea aphid

Herbivores that show host race formation on different plant species have proven to be valuable model systems for studying the evolution of specialization and speciation. Here, we use the pea aphid, Acyrthosiphon pisum, to investigate a possible link between specialization on two host plant species, Lotus uliginosus and Trifolium pratense, and resistance to a natural enemy, the fungal pathogen Erynia neoaphidis. Pea aphids collected on either plant species in the field showed in most cases poor survival on the alternate host plant. Furthermore, pea aphids specialized on T. pratense were very resistant to E. neoaphidis, whereas aphids specialized on L. uliginosus were susceptible. This susceptibility was not influenced by the actual food plant on which the assays were conducted. We discuss how selection from natural enemies may influence the process of specialization and race formation, and how specialization can affect the evolution of resistance.     

植物与植食性昆虫化学互作研究进展

植物与植食性昆虫之间存在着复杂的化学相互作用。一方面,当遭受植食性昆虫为害时,植物能识别植食性昆虫相关分子模式,触发早期信号事件和激素信号转导途径,并由此引起转录组与代谢组重组、直接和间接防御化合物含量升高,最后提高对植食性昆虫的抗性。另一方面,植食性昆虫也能识别植物的防御反应,并能通过分泌效应子、选贮、解毒以及降低敏感性等反防御措施抑制或适应植物的化学防御。深入剖析植物与植食性昆虫的化学互作,不仅可在理论上丰富对昆虫与植物互作关系的理解,而且可在实践上为作物害虫防控新技术的开发提供重要的理论与技术指导。     

A role of hexokinases in plant resistance to oxidative stress and pathogen infection

Previously, we reported that mitochondria-associated hexokinases are active in controlling programmed cell death in plants (Plant Cell 18, 2341-2355). Here, we investigated their role under abiotic- and biotic-stress conditions. Expression ofNbHxk1, aNicotiana benthamiana hexokinase gene, was stimulated by treatment with salicylic acid or methyl viologen (MV), and was also up-regulated by pathogen infection. In response to MV-induced oxidative stress, NbHxk1-silenced plants exhibited increased susceptibility, while the HXK1— and HXK2-overexpressingArabidopsis plants had enhanced tolerance. Moreover, those overexpressing plants showed greater resistance to the necrotrophic fungal pathogenAlternaria brassicicola. HXK-over-expression also mildly protected plants against the bacterial pathogenPseudomonas syringae pv.tomato DC3000, a response that was accompanied by increased H₂O₂ production and elevatedPR1 gene expression. These results demonstrate that higher levels of hexokinase confer improved resistance to MV-induced oxidative stress and pathogen infection.     

The essential role of fungal peroxisomes in plant infection

Several filamentous fungi are ecologically and economically important plant pathogens that infect a broad variety of crops. They cause high annual yield losses and contaminate seeds and fruits with mycotoxins. Not only powerful infection structures and detrimental toxins, but also cell organelles, such as peroxisomes, play important roles in plant infection. In this review, we summarize recent research results that revealed novel peroxisomal functions of filamentous fungi and highlight the importance of peroxisomes for infection of host plants. Central for fungal virulence are two primary metabolic pathways, fatty acid β-oxidation and the glyoxylate cycle, both of which are required to produce energy, acetyl-CoA, and carbohydrates. These are ultimately needed for the synthesis of cell wall polymers and for turgor generation in infection structures. Most novel results stem from different routes of secondary metabolism and demonstrate that peroxisomes produce important precursors and house various enzymes needed for toxin production and melanization of appressoria. All these peroxisomal functions in fungal virulence might represent elegant targets for improved crop protection.     

Antagonistic interactions between Aureobasidium pullulans and Fusarium culmorum,a fungal pathogen of winter wheat

The effect of the biological control agent Aureobasidium pullulans (de Bary) G. Arnaud on the development of Fusarium head blight (FHB) on winter wheat and kernel contamination with fungi of the genera Fusarium, Acremonium, Cladosporium and Penicillium was analyzed in a greenhouse experiment. Scanning electron microscopy was used to evaluate the distribution of A. pullulans cells and aggregates on wheat kernels, infection structures of Fusarium culmorum (W.G. Smith) Sacc and the antagonist-pathogen interactions. Biological control with A. pullulans reduced FHB severity by 21.67 % and improved grain filling by 5.02 %, compared with the control treatment. The survival of A. pullulans was good (to 31 cells per kernel), in particular on the surface and in the crease of kernels, including in pathogen-inoculated wheat plants. A. pullulans cells firmly adhered to F. culmorum hyphae, and damaged them. In most cases, autochthonous communities of filamentous fungi of the genera Acremonium and Penicillium developed at a slower rate after kernel inoculation with the pathogen.     

植物对昆虫不同防御类型及内在联系

植物与昆虫在长期的相互作用过程中,形成了复杂的防御体系。这个防御体系在时空方面都涉及多个层次,从而组成多个防御类型。本文首先总结了目前植物防御研究中的热点概念;而后根据文献并综合自己的研究,探讨了不同植物防御类型之间的相互关系,从机理上总结了各种植物防御类型的内在联系;最后,探讨了植物防御研究的发展趋势。本文从不同时空角度探讨了植物防御的概念及其相互关系,以期为研究者提供较为全面和深入的理论知识。     

Plant-mediated interactions between the rice water weevil and fall armyworm in rice

Greenhouse studies were conducted to investigate plant-mediated interactions between an above-ground and a below-ground herbivore when sharing a common host plant, rice (Oryza sativa L). Two common pests of rice were used: the rice water weevil (RWW), Lissorhoptrus oryzophilus Kuschel, as the root herbivore, and the fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith) as the foliage-feeding herbivore. Rice water weevil larval performance was assessed by measuring larval density and average weight in response to different levels of defoliation by FAW larvae. The reciprocal experiment was done to evaluate FAW performance (growth rate) in response to RWW feeding. Severe defoliation by FAW decreased RWW densities by 32% and reduced larval weights by 48% compared to larvae on roots of non-defoliated plants. Effects in the converse experiments were not as strong. FAW growth rates were reduced 9–37% when feeding on rice leaves from plants damaged by RWW compared to larvae feed leaves from the no damage treatment. These reciprocal negative effects show that RWW and FAW are potential competitors when sharing a rice plant. Because RWW and FAW did not interact directly, competition was plant-mediated.     

Variable responses of insects to hybrid versus parental sagebrush in common gardens

Both ecological and genetic mechanisms have been proposed to explain patterns of herbivore attack on interspecific plant hybrids, but distinguishing among them can be difficult in natural hybrid zones. We performed a common-garden experiment to evaluate four genetic hypotheses: dominance, additivity, elevated hybrid susceptibility, and elevated hybrid resistance. Censuses and cage experiments were used to compare insect responses to basin big sagebrush (Artemisia tridentata spp. tridentata), mountain big sagebrush (A. t. vaseyana), and their F₂ progeny. After two growing seasons, hybrid shrubs resembled mountain big sagenbrush in size, but were more similar to basin big sagebrush in flower production. Censuses of naturally colonizing insects (the gall midge Rhopalomyia obovata, the bagworm moth Apterona helix, and the aphid Obtusicauda coweni) tended to support the dominance hypothesis: if the insect clearly discriminated between the two parents, its frequency on hybrids closely resembled that on one of the parents. Moreover, colonization of hybrids in all three cases suggested a dominance deviation toward the susceptible parent rather than toward the resistant parent. In contrast to the censuses, cage experiments involving two insects supported the hybrid-susceptibility hypothesis; both survival and growth of the grasshopper Melanoplus sanguinipes and growth of the leaf beetle Trirhabda pilosa were higher on hybrid shrubs than on either parent. Because many secondary compounds have been determined to occur at intermediate concentrations in F₂ shrubs, dominance for susceptibility may indicate that insects respond to plant traits (e.g., oviposition stimulants and deterrents) in a threshold manner. Mechanisms underlying increased hybrid susceptibility are less clear, but our experimental design makes environmental explanations (e.g., the plant-stress hypothesis) unlikely. Although we eliminated several confounding factors, our results agree with the conclusion from natural hybrid zones that insect responses to hybrid plants are likely to be idiosyncratic; even congeneric species did not respond similarly to hybrid and parental plants.     

Potential applications of cryogenic technologies to plant genetic improvement and pathogen eradication

Rapid increases in human populations provide a great challenge to ensure that adequate quantities of food are available. Sustainable development of agricultural production by breeding more productive cultivars and by increasing the productive potential of existing cultivars can help meet this demand. The present paper provides information on the potential uses of cryogenic techniques in ensuring food security, including: (1) long-term conservation of a diverse germplasm and successful establishment of cryo-banks; (2) maintenance of the regenerative ability of embryogenic tissues that are frequently the target for genetic transformation; (3) enhancement of genetic transformation and plant regeneration of transformed cells, and safe, long-term conservation for transgenic materials; (4) production and maintenance of viable protoplasts for transformation and somatic hybridization; and (5) efficient production of pathogen-free plants. These roles demonstrate that cryogenic technologies offer opportunities to ensure food security.     

The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects

Plants are faced with a trade-off between on the one hand growth, development and reproduction and on the other hand defence against environmental stresses. Yet, research on insect-plant interactions has addressed plant-pollinator interactions and plant-attacker interactions separately. Plants have evolved a high diversity of constitutive and induced responses to attack, including the systemic emission of herbivore-induced plant volatiles (HIPVs). The effect of HIPVs on the behaviour of carnivorous insects has received ample attention for leaf-feeding (folivorous) species and their parasitoids and predators. Here, we review whether and to what extent HIPVs affect the interaction of plants in the flowering stage with mutualistic and antagonistic insects. Whereas the role of flower volatiles in the interactions between plants and insect pollinators has received increased attention over the last decade, studies addressing both HIPVs and pollinator behaviour are rare, despite the fact that in a number of plant species herbivory is known to affect flower traits, including size, nectar secretion and composition. In addition, folivory and florivory can also result in significant changes in flower volatile emission and in most systems investigated, pollinator visitation decreased, although exceptions have been found. Negative effects of HIPVs on pollinator visitation rates likely exert negative selection pressure on HIPV emission. The systemic nature of herbivore-induced plant responses and the behavioural responses of antagonistic and mutualistic insects, requires the study of volatile emission of entire plants in the flowering stage. We conclude that approaches to integrate the study of plant defences and pollination are essential to advance plant biology, in particular in the context of the trade-off between defence and growth/reproduction.