How do aphids respond to elevated CO2?

The performance of herbivore insects is determined directly by the quality of host plants. Elevated CO₂ induced a decline in foliar nitrogen, which reduced the growth of chewing insects. Phloem-sucking insects (i.e. aphid), however, had species-specific responses to elevated CO₂ and were the only feeding guild to respond positively to elevated CO₂. Although many studies attempt to illuminate the interaction between aphids and plants under elevated CO₂, few studies can explain why some aphids are more successful than other chewing insects in elevated CO₂. Elevated CO₂ leads to a re-allocation of the carbon and nitrogen resources in plant tissue, which increases the thickness of the microscopic structures of leaves, reduces amino acids content of leaf phloem sap and increases the secondary metabolites. Considering the complexity of aphid–plant interactions, it is difficult and unreasonable to predict the general response of aphids to elevated CO₂ using a single plant component. Instead, it is more likely that aphids are able to overcome the disadvantages of the indirect effects of elevated CO₂ by reducing developmental times and increasing fecundity under elevated CO₂ conditions. Our results provide several clues to why some aphids are successful in elevated CO₂ conditions. We review recent studies of the effects of elevated CO₂ on aphids and discuss the effects of elevated CO₂ on aphid performance on crops using cotton and cereal aphids as examples.     

Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects

Plant responses to enemies are coordinated by several interacting signaling systems. Molecular and genetic studies with mutants and exogenous signal application suggest that jasmonate (JA)-, salicylate (SA)-, and ethylene (ET)-mediated pathways modulate expression of portions of the defense phenotype in Arabidopsis (Arabidopsis thaliana), but have not yet linked these observations directly with plant responses to insect attack. We compared the glucosinolate (GS) profiles of rosette leaves of 4-week-old mutant and transgenic Arabidopsis (Columbia) plants compromised in these three major signaling pathways, and characterized responses by those plants to feeding by two phloem-feeding aphids (generalist Myzus persicae and specialist Brevicoryne brassicae) and one generalist caterpillar species (Spodoptera exigua Hubner). Blocked JA signaling in coronatine-insensitive (coi1) and enhanced expression of SA-signaled disease resistance in hypersensitive response-like (hrl1) mutants reduced constitutive GS concentrations, while blocking SA signaling at the mediator protein npr1 mutant (NPR) increased them. There was no significant impact on constitutive GS contents of blocking ET signaling (at ET resistant [etr1]) or reducing SA concentrations (nahG transgene). We found increased GS accumulation in response to insect feeding, which required functional NPR1 and ETR1 but not COI1 or SA. Insect feeding caused increases primarily in short-chain aliphatic methylsulfinyl GS. By contrast, responses to exogenous JA, a frequent experimental surrogate for insect attack, were characterized by an increase in indolyl GS. Insect performance, measured as population increase or weight increase, was negatively related to GS levels, but we found evidence that other, ET-regulated factors may also be influential. Plant resistance to (consumption by) S. exigua was not related to insect growth because some plant chemistries inhibited growth while others inhibited feeding. These major signaling pathways modulate Arabidopsis GS accumulation and response to both phloem-feeding and chewing insects, often antagonistically; NPR appears to be central to these interactions. Our results indicate that exogenous signal application and plant consumption measures may not provide useful measures of plant responses to actual insect feeding.     

Activation of ethylene‐related genes in response to aphid feeding on resistant and susceptible melon and tomato plants

The simple gaseous compound ethylene (ET) has long been recognized as a common component of plant responses to insect feeding and pathogen attack. However, it is presently uncertain whether it plays a role in host–plant resistance to piercing–sucking insects such as aphids. In these experiments, we investigated the expression of key ET‐associated genes in resistant and susceptible interactions in two model systems: the tomato‐Mi‐Macrosiphum euphorbiae (Thomas) (Hemiptera: Aphididae: Macrosiphini) system and the melon‐virus aphid transmission gene (Vat)‐Aphis gossypii Glover (Hemiptera: Aphididiae: Aphidini) system. We examined expression patterns of genes associated with ET synthesis, perception, signal transduction, and downstream response. When compared with control plants, plants infested with aphids showed marked differences in gene expression. In particular, ET signaling pathway genes and downstream response genes were highly upregulated in the resistant interaction between A. gossypii and Vat⁺, indicating ET may play a role in Vat‐mediated host–plant resistance. A key integrator between the ET and jasmonic acid pathways (Cm‐ERF1) showed the strongest response.     

Evolution of jasmonate and salicylate signal crosstalk

The evolution of land plants approximately 470 million years ago created a new adaptive zone for natural enemies (attackers) of plants. In response to attack, plants evolved highly effective, inducible defense systems. Two plant hormones modulating inducible defenses are salicylic acid (SA) and jasmonic acid (JA). Current thinking is that SA induces resistance against biotrophic pathogens and some phloem feeding insects and JA induces resistance against necrotrophic pathogens, some phloem feeding insects and chewing herbivores. Signaling crosstalk between SA and JA commonly manifests as a reciprocal antagonism and may be adaptive, but this remains speculative. We examine evidence for and against adaptive explanations for antagonistic crosstalk, trace its phylogenetic origins and provide a hypothesis-testing framework for future research on the adaptive significance of SA-JA crosstalk.     

Jasmonate-dependent plant defenses mediate soybean thrips and soybean aphid performance on soybean

Insect herbivores from different feeding guilds induce different signaling pathways in plants. In this study, we examined the effects of salicylic acid (SA)- and jasmonic acid (JA)-mediated defenses on performance of insect herbivores from two different feeding guilds: cell-content feeders, soybean thrips and phloem feeders, soybean aphids. We used a combination of RT-qPCR analysis and elicitor-induced plant resistance to determine induction of SA and JA signaling pathways and the impact on herbivore performance. In the early interaction between the host plant and the two herbivores, SA and JA signaling seems to occur simultaneously. But overall, soybean thrips induced JA-related marker genes, whereas soybean aphids increased SA and ABA-related marker genes over a 24-h period. Populations of both soybean thrips and soybean aphids were reduced (47 and 25 %, respectively) in methyl jasmonate (MeJA)-pretreated soybean plants. SA treatment has no effect on either herbivore performance. A combination pretreatment of SA and MeJA did not impact soybean thrips population but reduced soybean aphid numbers which was comparable with MeJA treatment. Our data suggest that SA–JA antagonism could be responsible for the effect of hormone pretreatment on thrips performance, but not on aphid performance. By linking plant defense gene expression and elicitor-induced resistance, we were able to pinpoint the role for JA signaling pathway in resistance to two herbivores from different feeding guilds.     

Evaluation of Greenbug and Yellow Sugarcane Aphid Feeding Behavior on Resistant and Susceptible Switchgrass Cultivars

Switchgrass (Panicum virgatum L.) is an emerging biofuel crop that serves as host for aphids. To discern the effects of plant age and possible resistance mechanisms, the feeding behavior of greenbugs (Schizaphis graminum Rondani.) and the yellow sugarcane aphid (Sipha flava Forbes.) was monitored on three diverse switchgrasses by the electrical penetration graph (EPG) technique. Callose deposition and genes associated with callose metabolism were also analyzed to discern their association with plant resistance. There was a strong host effect on greenbugs feeding on lowland cultivar Kanlow at the V3 stage of development, as compared to the greenbug-susceptible upland cultivar Summer and plants derived from Kanlow (♂) × Summer (♀) (K×S) crosses. These data confirmed that Kanlow at the V3 stage had antibiosis to greenbugs, which was absent in the Summer and K×S plants. In contrast, similar effects were not observed for yellow sugarcane aphids, excluding significant differences in the time to first probe on Kanlow plants at the V1 stage and reduction in time spent on pathway processes on Kanlow plants at the V3 stage. These data demonstrated that Kanlow plants may have multiple sources of resistance to the two aphids, and possibly some were phloem based. Microscopy of leaf sections stained with aniline blue for callose was suggestive of increased callose deposition in the sieve elements in Kanlow plants relative to Summer and K×S plants. RT-qPCR analysis of several genes associated with callose metabolism in infested plants was equivocal. Overall, these studies suggest the presence of multiple defense mechanisms against aphids in Kanlow plants, relative to Summer and K×S plants.     

The Myriad Plant Responses to Herbivores

Abstract Plant responses to herbivores are complex. Genes activated on herbivore attack are strongly correlated with the mode of herbivore feeding and the degree of tissue damage at the feeding site. Phloem-feeding whiteflies and aphids that produce little injury to plant foliage are perceived as pathogens and activate the salicylic acid (SA)-dependent and jasmonic acid (JA)/ethylene-dependent signaling pathways. Differential expression of plant genes in response to closely related insect species suggest that some elicitors generated by phloem-feeding insects are species-specific and are dependent on the herbivore's developmental stage. Other elicitors for defense-gene activation are likely to be more ubiquitous. Analogies to the pathogen-incompatible reactions are found. Chewing insects such as caterpillars and beetles and cell-content feeders such as mites and thrips cause more extensive tissue damage and activate wound-signaling pathways. Herbivore feeding is not equivalent to mechanical wounding. Wound responses are a part of the induced responses that accompany herbivore feeding. Herbivores induce direct defenses that interfere with herbivore feeding, growth and development, fecundity, and fertility. In addition, herbivores induce an array of volatiles that creates an indirect mechanism of defense. Volatile blends provide specific cues to attract herbivore parasites and predators to infested plants. The nature of the elicitors for volatile production is discussed.     

植物和刺吸式口器昆虫的诱导防御与反防御研究进展

刺吸式口器昆虫在长期的进化过程中形成特殊的口针结构,用于专门吸食植物韧皮部筛管细胞的汁液成分.以蚜虫为例,它们在取食过程中分泌的胶状唾液和水状唾液将有效的降低植物防御反应,其中水状唾液包含的大量酶类不仅可以帮助蚜虫穿刺植物韧皮部,刺探到筛管细胞,同时也是植物感受蚜虫为害的激发因子,诱导出植物防御反应和相关抗性基因的表达...     

UV‐B impact on aphid performance mediated by plant quality and plant changes induced by aphids

Plants face various abiotic and biotic environmental factors and therefore need to adjust their phenotypic traits on several levels. UV‐B radiation is believed to impact herbivorous insects via host plant changes. Plant responses to abiotic challenges (UV‐B radiation) and their interaction with two aphid species were explored in a multifactor approach. Broccoli plants [Brassica oleracea L. convar. botrytis (L.), Brassicaceae] were grown in two differently covered greenhouses, transmitting either 80% (high UV‐B) or 4% (low UV‐B) of ambient UV‐B. Three‐week‐old plants were infested with either specialist cabbage aphids [Brevicoryne brassicae (L.), Sternorrhyncha, Aphididae] or generalist green peach aphids [Myzus persicae (Sulzer), Sternorrhyncha, Aphididae]. Plants grown under high‐UV‐B intensities were smaller and had higher flavonoid concentrations. Furthermore, these plants had reduced cuticular wax coverage, whereas amino acid concentrations of the phloem sap were little influenced by different UV‐B intensities. Cabbage aphids reproduced less on plants grown under high UV‐B than on plants grown under low UV‐B, whereas reproduction of green peach aphids in both plant light sources was equally poor. These results are likely related to the different specialisation‐dependent sensitivities of the two species. The aphids also affected plant chemistry. High numbers of cabbage aphid progeny on low‐UV‐B plants led to decreased indolyl glucosinolate concentrations. The induced change in these glucosinolates may depend on an infestation threshold. UV‐B radiation considerably impacts plant traits and subsequently affects specialist phloem‐feeding aphids, whereas aphid growth forces broccoli to generate specific defence responses.     

Elevated CO2 alters the feeding behaviour of the pea aphid by modifying the physical and chemical resistance of Medicago truncatula

Elevated CO₂ compromises the resistance of leguminous plants against chewing insects, but little is known about whether elevated CO₂ modifies the resistance against phloem‐sucking insects or whether it has contrasting effects on the resistance of legumes that differ in biological nitrogen fixation. We tested the hypothesis that the physical and chemical resistance against aphids would be increased in Jemalong (a wild type of Medicago truncatula) but would be decreased in dnf1 (a mutant without biological nitrogen fixation) by elevated CO₂. The non‐glandular and glandular trichome density of Jemalong plants increased under elevated CO₂, resulting in prolonged aphid probing. In contrast, dnf1 plants tended to decrease foliar trichome density under elevated CO₂, resulting in less surface and epidermal resistance to aphids. Elevated CO₂ enhanced the ineffective salicylic acid‐dependent defence pathway but decreased the effective jasmonic acid/ethylene‐dependent defence pathway in aphid‐infested Jemalong plants. Therefore, aphid probing time decreased and the duration of phloem sap ingestion increased on Jemalong under elevated CO₂, which, in turn, increased aphid growth rate. Overall, our results suggest that elevated CO₂ decreases the chemical resistance of wild‐type M. truncatula against aphids, and that the host's biological nitrogen fixation ability is central to this effect.     

Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid)

The cleavage of glucosinolates by myrosinase to produce toxic breakdown products is a characteristic insect defense of cruciferous plants. Although green peach aphids ( Myzus persicae ) are able to avoid most contact with myrosinase when feeding from the phloem of Arabidopsis thaliana , indole glucosinolates are nevertheless degraded during passage through the insects. A defensive role for indole glucosinolates is suggested by the observation that atr1D mutant plants, which overproduce indole glucosinolates, are more resistant to M. persicae , whereas cyp79B2 cyp79B3 double mutants, which lack indole glucosinolates, succumb to M. persicae more rapidly. Indole glucosinolate breakdown products, including conjugates formed with ascorbate, glutathione and amino acids, are elevated in the honeydew of M. persicae feeding from atr1D mutant plants, but are absent when the aphids are feeding on cyp79B2 cyp79B3 double mutants. M. persicae feeding from wild-type plants and myrosinase-deficient tgg1 tgg2 double mutants excrete a similar profile of indole glucosinolate-derived metabolites, indicating that the breakdown is independent of these foliar myrosinases. Artificial diet experiments show that the reaction of indole-3-carbinol, a breakdown product of indol-3-ylmethylglucosinolate, with ascorbate, glutathione and cysteine produces diindolylmethylcysteines and other conjugates that have antifeedant effects on M. persicae . Therefore, the post-ingestive breakdown of indole glucosinolates provides a defense against herbivores such as aphids that can avoid glucosinolate activation by plant myrosinases.     

Field evidence for indirect interactions between foliar‐feeding insect and root‐feeding nematode communities on Nicotiana tabacum

Abstract 1. As herbivory often elicits systemic changes in plant traits, indirect interactions via induced plant responses may be a pervasive feature structuring herbivore communities. Although the importance of this phenomenon has been emphasised for herbivorous insects, it is unknown if and how induced responses contribute to the organisation of other major phytoparasitic taxa. 2. Survey and experimental field studies were used to investigate the role of plants in linking the dynamics of foliar‐feeding insects and root‐feeding nematodes on tobacco, Nicotiana tabacum. 3. Plant‐mediated interactions between insects and nematodes could largely be differentiated by insect feeding guild, with positive insect–nematode interactions predominating with leaf‐chewing insects (caterpillars) and negative interactions occurring with sap‐feeding insects (aphids). For example, insect defoliation was positively correlated with the abundance of root‐feeding nematodes, but aphids and nematodes were negatively correlated. Experimental field manipulations of foliar insect and nematode root herbivory also tended to support this outcome. 4. Overall, these results suggest that plants indirectly link the dynamics of divergent consumer taxa in spatially distinct ecosystems. This lends support to the growing perception that plants play a critical role in propagating indirect effects among a diverse assemblage of consumers.     

The molecular bases of plant resistance and defense responses to aphid feeding: current status

Plant genes participating in the recognition of aphid herbivory in concert with plant genes involved in defense against herbivores mediate plant resistance to aphids. Several such genes involved in plant disease and nematode resistance have been characterized in detail, but their existence has only recently begun to be determined for arthropod resistance. Hundreds of different genes are typically involved and the disruption of plant cell wall tissues during aphid feeding has been shown to induce defense responses in Arabidopsis, Triticum, Sorghum, and Nicotiana species. Mi‐1.2, a tomato gene for resistance to the potato aphid, Macrosiphum euphorbiae (Thomas), is a member of the nucleotide‐binding site and leucine‐rich region Class II family of disease, nematode, and arthropod resistance genes. Recent studies into the differential expression of Pto‐ and Pti1‐like kinase genes in wheat plants resistant to the Russian wheat aphid, Diuraphis noxia (Mordvilko), provide evidence of the involvement of the Pto class of resistance genes in arthropod resistance. An analysis of available data suggests that aphid feeding may trigger multiple signaling pathways in plants. Early signaling includes gene‐for‐gene recognition and defense signaling in aphid‐resistant plants, and recognition of aphid‐inflicted cell damage in both resistant and susceptible plants. Furthermore, signaling is mediated by several compounds, including jasmonic acid, salicylic acid, ethylene, abscisic acid, giberellic acid, nitric oxide, and auxin. These signals lead to the development of direct chemical defenses against aphids and general stress‐related responses that are well characterized for a number of abiotic and biotic stresses. In spite of major plant taxonomic differences, similarities exist in the types of plant genes expressed in response to feeding by different species of aphids. However, numerous differences in plant signaling and defense responses unique to specific aphid–plant interactions have been identified and warrant further investigation.     

How nutritionally imbalanced is phloem sap for aphids?

Aphids harbour intracellular symbionts (Buchnera) that provide their host with amino acids present in low amounts in their diet, phloem sap. To find out the extent to which aphids depend on their symbionts for synthesis of individual essential amino acids, we have evaluated how well phloem sap amino acid composition matches the aphids' needs. Amino acid compositions of the ingested phloem sap were compared to amino acids in aphid body proteins and also to available information about optimal diet composition for other plant feeding insects. Phloem sap data from severed stylets of two aphid species, Rhopalosiphum padi (L.) (Homoptera: Aphididae) feeding on wheat, and Uroleucon sonchi (L.) (Homoptera: Aphididae) feeding on Sonchus oleraceus (L.), together with published information on phloem sap compositions from other plant species were used.Phloem sap has in general only around 20% essential amino acids, with a range from 15–48%. Aphid body proteins and optimal diets for two other plant feeding insects have around 50%. The phloem sap of early flowering S. oleraceus ingested by U. sonchi contained 48%, which seems to be exceptional. Aphids feeding on different plants appear to be very differently dependent on their symbionts for their overall essential amino acid synthesis, due to the large variation in proportion of essential amino acids in phloem sap from different plants.The profile of the essential amino acids in phloem sap from different plant species corresponds rather well to profiles of both aphid body proteins and optimal diets determined for plant feeding insects. However, methionine and leucine in phloem sap are in general low in these comparisons, suggesting a higher dependence on the symbiont for synthesis of these amino acids. Concentrations of several essential amino acids in phloem from different plant species seem to vary together, suggesting that levels of symbiont provisioning of different amino acids are adjusted in parallel.     

Linking belowground and aboveground phenology in two boreal forests in Northeast China

Plants are frequently attacked by both pathogens and insects, and an attack from one can induce plant responses that affect resistance to the other. However, we currently lack a predictive framework for understanding how pathogens, their vectors, and other herbivores interact. To address this gap, we have investigated the effects of a viral infection in the host plant on both its aphid vector and non-vector herbivores. We tested whether the infection by three different strains of Potato virus Y (PVY^NTN, PVY^NO and PVY^O) on tomato plants affected: (1) the induced plant defense pathways; (2) the abundance and fecundity of the aphid vector (Macrosiphum euphorbiae); and (3) the performance of two non-vector species: a caterpillar (Trichoplusia ni) and a beetle (Leptinotarsa decemlineata). While infection by all three strains of PVY induced the salicylate pathway, PVY^NTN induced a stronger and longer response. Fecundity and density of aphids increased on all PVY-infected plants, suggesting that the aphid response is not negatively associated with salicylate induction. In contrast, the performance of non-vector herbivores positively correlated with the strength of salicylate induction. PVY^NTN infection decreased plant resistance to both non-vector herbivores, increasing their growth rates. We also demonstrated that the impact of host plant viral infection on the caterpillar results from host plant responses and not the effects of aphid vector feeding. We propose that pathogens chemically mediate insect–plant interactions by activating the salicylate pathway and decreasing plant resistance to chewing insects, which has implications for both disease transmission and insect community structure.     

Aphid responses to volatile cues from turnip plants (Brassica rapa) infested with phloem-feeding and chewing herbivores

Herbivore-induced plant volatiles provide foraging cues for herbivores and for herbivores’ natural enemies. Aphids induce plant volatile emissions and also utilize plant-derived olfactory volatile cues, but the chemical ecology of aphids and other phloem-feeding insects is less extensively documented than that of chewing insects. Here, we characterize the volatile cues emitted by turnip plants (Brassica rapa) under attack by an aphid (Myzus persicae) or by the chewing lepidopteran larva Heliothis virescens. We also tested the behavioral responses of M. persicae individuals to the odors of undamaged and herbivore-damaged plants presented singly or in combination, as well as to the odor of crushed conspecifics (simulating predation). Gas chromatographic analysis of the volatile blend of infested turnips revealed distinct profiles for both aphid- and caterpillar-induced plants, with induced compounds including green-leaf alcohols, esters, and isothiocyanates. In behavioral trials, aphids exhibited increased activity in the presence of plant odors and positive attraction to undamaged turnip plants. However, aphids exhibited a strong preference for the odors of healthy versus plants subjected to herbivore damage, and neither aphid- or caterpillar-damaged plants were attractive compared to clean-air controls. Reduced aphid attraction to herbivore-infested plants may be mediated by changes in the volatile blend constituent composition, including large amounts of isothiocyanates and green-leaf volatiles or, in the case of aphid-infested plants, of the aphid alarm pheromone, (E)-β-farnesene.