Understanding the Plant Aphid Interaction: A Review

The interaction between plant-aphid is phenomenal and complex. Aphids possess efficient mouthparts which feed on plant sap intensively. Adaptation to host plants and successful feeding is achieved through the strategic ability of aphids to reproduce sexually and asexually (parthenogenesis). Aphid infestation damages the plant in diverse ways and induces plant defense. Though plant elicit direct and indirect defense to resist aphid feeding, the effectiveness of plant resistance depends largely on the aphid infestation rate and quality of the host plant. To control aphid infestation and plant damage, dependency on insecticides is undesirable due to insecticidal resistance of aphids and environmental pollution. The approach towards the development of the genetically engineered crops which are aphid resistant can be the considerable potential to aphid control..

The effects of condensed tannins on behaviour and performance of a specialist aphid on Aspen

The plant defence syndromes (PDSs) concept predicts host plants should develop diverse resistance profiles against their herbivores. We used Electrical Penetration Graphs (EPG) to investigate complex and genotype-specific penetration-barriers to Chaitophorous tremulae aphid feeding on Aspen (Populus tremula). Leaf condensed tannins were associated with enhanced probing activity and increased ingestion of xylem sap. Aphids probed less on Aspen genotypes low in tannins, suggesting other defence traits might be elicited. Our results support the idea of multi-layered PDS defence traits, and provide evidence of high plasticity in tannin profiles across temporal and spatial scales. We conclude that tannin plasticity may form a dynamically unpredictable aspect of the PDS defence arsenal that protects Aspen against piercing-sucking aphids.

The Effectiveness of Physical and Chemical Defense Responses of Wild Emmer Wheat Against Aphids Depends on Leaf Position and Genotype

The bird cherry-oat aphid (Rhopalosiphum padi) is one of the most destructive insect pests in wheat production. To reduce aphid damage, wheat plants have evolved various chemical and physical defense mechanisms. Although these mechanisms have been frequently reported, much less is known about their effectiveness. The tetraploid wild emmer wheat (WEW; Triticum turgidum ssp. dicoccoides), one of the progenitors of domesticated wheat, possesses untapped resources from its numerous desirable traits, including insect resistance. The goal of this research was to determine the effectiveness of trichomes (physical defense) and benzoxazinoids (BXDs; chemical defense) in aphid resistance by exploiting the natural diversity of WEW. We integrated a large dataset composed of trichome density and BXD abundance across wheat genotypes, different leaf positions, conditions (constitutive and aphid-induced), and tissues (whole leaf and phloem sap). First, we evaluated aphid reproduction on 203 wheat accessions and found large variation in this trait. Then, we chose eight WEW genotypes and one domesticated durum wheat cultivar for detailed quantification of the defense mechanisms across three leaves. We discovered that these defense mechanisms are influenced by both leaf position and genotype, where aphid reproduction was the highest on leaf-1 (the oldest), and trichome density was the lowest. We compared the changes in trichome density and BXD levels upon aphid infestation and found only minor changes relative to untreated plants. This suggests that the defense mechanisms in the whole leaf are primarily anticipatory and unlikely to contribute to aphid-induced defense. Next, we quantified BXD levels in the phloem sap and detected a significant induction of two compounds upon aphid infestation. Moreover, evaluating aphid feeding patterns showed that aphids prefer to feed on the oldest leaf. These findings revealed the dynamic response at the whole leaf and phloem levels that altered aphid feeding and reproduction. Overall, they suggested that trichomes and the BXD 2,4-dihydroxy-7- methoxy-1,4-benzoxazin-3-one (DIMBOA) levels are the main factors determining aphid resistance, while trichomes are more effective than BXDs. Accessions from the WEW germplasm, rich with trichomes and BXDs, can be used as new genetic sources to improve the resistance of elite wheat cultivars.

Cowpea Aphid Resistance In Cowpea Line CB77 Functions Primarily Through Antibiosis And Eliminates Phytotoxic Symptoms of Aphid Feeding

Cowpea (Vigna unguiculata) is one of the most important crops in semiarid areas of the world, where it thrives in hot, dry conditions. While cowpea is able to withstand abiotic stresses, it suffers serious losses from biotic antagonists, including infestation by the cowpea aphid (Aphis craccivora). Cowpea aphid infestations are highly destructive, especially on young plants. However, it is unclear whether cowpea aphid damage is the result of aphids having phytotoxic effects on their hosts, or simple density effects. To better understand cowpea aphid damage and the potential for resistance traits to mitigate aphid impacts, we evaluated phenotypic changes in cowpea in response to variable aphid densities and systemic versus local infestations. Low aphid densities induced leaf distortions and pseudogalling, suggesting that cowpea aphids are phytotoxic to cowpea. Resistance to the cowpea aphid has been previously identified in an African cowpea germplasm, and near isogenic lines (NILs) containing resistance quantitative trait loci (QTL) were generated in the California blackeye cultivar background. Using a series of performance assays, we determined that resistance conferred by the two QTL counteracts aphid phytotoxicity and severely limits aphid growth and fecundity. Using choice assays, a preference by cowpea aphids for the susceptible NIL was observed. Electrical penetration graph analysis revealed that the resistance phenotype includes weak surface level deterrence and strong phloem based resistance that manifests during the sap ingestion phase. Our study provides evidence of phytotoxic traits in A. craccivora while identifying a viable means of counteracting aphid damage and reproductive potential through resistance.

Diuraphis noxia (Russian wheat aphid).

D. noxia has a great economic impact on cereal crops (Brooks et al., 1994). It is a phloem feeder like other aphids and the symptoms evident on plants are a result of this feeding mechanism. By feeding on the phloem, the aphid damages the plants through nutrient drainage (Dixon, 1985) which results in chlorosis, necrosis, wilting, stunting, and curling of the leaves, misshapen or nonappearance of new growth, and localised cell death at the site of aphid feeding. D. noxia further elicits an increase in essential amino acids in the phloem sap by triggering the breakdown of proteins in infested wheat leaves (Burd and Burton, 1992; du Toit, 1986; Ma et al., 1998; Miller et al., 2001). The damage to the foliar tissue is thought to play a role in the pest's ability to increase nutritional quality of the host plant (Botha et al., 2006).

Biochemical markers of oxidative stress in maize seedlings exposed to rose-grass aphids

We studied the influence of rose-grass aphid (Metopolophium dirhodum L.) infestation on the biochemical markers of oxidative stress in seedlings of two maize (Zea mays L.) varieties (relatively resistant Ambrozja and resistant Plomyk). We compared the generation of superoxide anion radicals O2-, level of hydrogen peroxide (H2O2), lipid peroxidation products (MDA) as well as markers of protein damage (protein-bound carbonyl groups). The studied parameters were measured at 24, 48, 72 and 96 h post-initial aphid infestation compared to the non-infested control seedlings. Our studies indicated that the rose-grass aphid feeding evoked oxidative stress in the maize seedlings. Investigated Z. mays cultivars exhibited excessive generation of superoxide anion radicals in response to insect treatments. Rose-grass aphid feeding increased the H2O2 level in maize tissues with similar levels observed at most periods post-infestation with M. dirhodum, also increased lipid peroxidation products with the maximal levels at 48 and 72 h for Ambrozja and 48, 72 and 96 h post-infestation for Plomyk varieties. Further at 48 and 72 h post-initial aphid infestation, there was an increase in protein bound carbonyl groups content in the maize seedlings after infestation with aphids.

Induced Local and Systemic Defense Responses in Tomato Underlying Interactions Between the Root-Knot Nematode Meloidogyne incognita and the Potato Aphid Macrosiphum euphorbiae

Plants mediate interactions between different herbivores that attack simultaneously or sequentially aboveground (AG) and belowground (BG) organs. The local and systemic activation of hormonal signaling pathways and the concomitant accumulation of defense metabolites underlie such AG-BG interactions. The main plant-mediated mechanisms regulating these reciprocal interactions via local and systemic induced responses remain poorly understood. We investigated the impact of root infection by the root-knot nematode (RKN) Meloidogyne incognita at different stages of its infection cycle, on tomato leaf defense responses triggered by the potato aphid Macrosiphum euphorbiae. In addition, we analyzed the reverse impact of aphid leaf feeding on the root responses triggered by the RKN. We focused specifically on the signaling pathways regulated by the phytohormones jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), and indole-3-acetic acid (IAA) as well as steroidal glycoalkaloids as induced defense compounds. We found that aphid feeding did not induce AG hormonal signaling, but it repressed steroidal glycoalkaloids related responses in leaves, specifically when feeding on plants in the vegetative stage. Root infection by the RKN impeded the aphid-triggered repression of the steroidal glycoalkaloids-related response AG. In roots, the RKN triggered the SA pathway during the entire infection cycle and the ABA pathway specifically during its reproduction stage. RKN infection also elicited the steroidal glycoalkaloids related gene expression, specifically when it was in the galling stage. Aphid feeding did not systemically alter the RKN-induced defense responses in roots. Our results point to an asymmetrical interaction between M. incognita and Ma. euphorbiae when co-occurring in tomato plants. Moreover, the RKN seems to determine the root defense response regardless of a later occurring attack by the potato aphid AG.

Transgenic Expression of dsRNA Targeting the Pentalonia nigronervosa acetylcholinesterase Gene in Banana and Plantain Reduces Aphid Populations

The banana aphid, Pentalonia nigronervosa, is the sole insect vector of banana bunchy top virus (BBTV), the causal agent of banana bunchy top disease. The aphid acquires and transmits BBTV while feeding on infected banana plants. RNA interference (RNAi) enables the generation of pest and disease-resistant crops; however, its effectiveness relies on the identification of pivotal gene sequences to target and silence. Acetylcholinesterase (AChE) is an essential enzyme responsible for the hydrolytic metabolism of the neurotransmitter acetylcholine in animals. In this study, the AChE gene of the banana aphid was targeted for silencing by RNAi through transgenic expression of AChE dsRNA in banana and plantain plants. The efficacy of dsRNA was first assessed using an artificial feeding assay. In vitro aphid feeding on a diet containing 7.5% sucrose, and sulfate complexes of trace metals supported aphid growth and reproduction. When AChE dsRNA was included in the diet, a dose of 500 ng/μL was lethal to the aphids. Transgenic banana cv. Cavendish Williams and plantain cvs. Gonja Manjaya and Orishele expressing AChE dsRNA were regenerated and assessed for transgene integration and copy number. When aphids were maintained on elite transgenic events, there was a 67.8%, 46.7%, and 75.6% reduction in aphid populations growing on Cavendish Williams, Gonja Manjaya, and Orishele cultivars, respectively, compared to those raised on nontransgenic control plants. These results suggest that RNAi targeting an essential aphid gene could be a useful means of reducing both aphid infestation and potentially the spread of the disease they transmit.

Non-Target Effects of dsRNA Molecules in Hemipteran Insects

Insect pest control by RNA interference (RNAi)-mediated gene expression knockdown can be undermined by many factors, including small sequence differences between double-stranded RNA (dsRNA) and the target gene. It can also be compromised by effects that are independent of the dsRNA sequence on non-target organisms (known as sequence-non-specific effects). This study investigated the species-specificity of RNAi in plant sap-feeding hemipteran pests. We first demonstrated sequence-non-specific suppression of aphid feeding by dsRNA at dietary concentrations ≥0.5 µg µL−1. Then we quantified the expression of NUC (nuclease) genes in insects administered homologous dsRNA (with perfect sequence identity to the target species) or heterologous dsRNA (generated against a related gene of non-identical sequence in a different insect species). For the aphids Acyrthosiphon pisum and Myzus persicae, significantly reduced NUC expression was obtained with the homologous but not heterologous dsRNA at 0.2 µg µL−1, despite high dsNUC sequence identity. Follow-up experiments demonstrated significantly reduced expression of NUC genes in the whitefly Bemisia tabaci and mealybug Planococcus maritimus administered homologous dsNUCs, but not heterologous aphid dsNUCs. Our demonstration of inefficient expression knockdown by heterologous dsRNA in these insects suggests that maximal dsRNA sequence identity is required for RNAi targeting of related pest species, and that heterologous dsRNAs at appropriate concentrations may not be a major risk to non-target sap-feeding hemipterans.

Genetic structure of Malus sylvestris and potential link with preference/performance by the rosy apple aphid pest Dysaphis plantaginea

The European crabappleMalus sylvestris, a crop wild relative ofMalus domestica, is a major contributor to the cultivated apple genome and represents a potential source of interesting alleles or genes, particularly pest resistance traits. An original approach was used to explore the trophic interaction betweenM. sylvestrispopulations and its pest, the rosy apple aphid (Dysaphis plantaginea). Using 13 microsatellite markers, population genetic structure and level of crop-to-wild introgressions were inferred betweenM. sylvestrisseedlings from three sites in Europe (Denmark, France, Romania), andM. domesticaseedlings. Genetically characterized plants were also used to analyze aphid feeding behavior and fitness parameters. First, aphids submitted to two genetically closeM. sylvestrispopulations (the Danish and French) exhibited similar behavioral parameters, suggesting similar patterns of resistance in these host plants. Second, the RomanianM. sylvestrispopulation was most closely genetically related toM. domestica. Although the two plant genetic backgrounds were significantly differentiated, they showed comparable levels of sensitivity toD. plantagineainfestation. Third, aphid fitness parameters were not significantly impacted by the host plant’s genetic background. Finally, crop-to-wild introgression seemed to significantly drive resistance toD. plantagineaindependent of host plant population genetic structure, with hybrids being less suitable hosts.