Avirulent Aphids Research Articles

Exploring the Dynamics of Virulent and Avirulent Aphids: A Case for a 'Within Plant' Refuge.

The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is an invasive pest that can cause severe yield loss to soybeans in the North Central United States. A tactic to counter this pest is the use of aphid-resistant soybean varieties. However, the frequency of virulent biotypes that can survive on resistant varieties is expected to increase as more farmers use these varieties. Soybean aphids can alter soybean physiology primarily by two mechanisms, feeding facilitation, and the obviation of resistance, favoring subsequent colonization by additional conspecifics. We developed a nonlocal, differential equation population model to explore the dynamics of these biological mechanisms on soybean plants coinfested with virulent and avirulent aphids. We then use demographic parameters from laboratory experiments to perform numerical simulations via the model. We used this model to determine that initial conditions are an important factor in the season-long cooccurrence of both biotypes. The initial population of both biotypes above the resistance threshold or avirulent aphid close to resistance threshold and high virulent aphid population results in coexistence of the aphids throughout the season. These simulations successfully mimicked aphid dynamics observed in the field- and laboratory-based microcosms. The model showed an increase in colonization of virulent aphids increases the likelihood that aphid resistance is suppressed, subsequently increasing the survival of avirulent aphids. This interaction produced an indirect, positive interaction between the biotypes. These results suggest the potential for a ‘within plant’ refuge that could contribute to the sustainable use of aphid-resistant soybeans.

Evaluating the role of insecticidal seed treatment and refuge for managing soybean aphid virulence.

Managing insect virulence can extend the durability of host-plant resistant crops. Genetically modified resistant crops continue to be successful because of insect-resistant management strategies that delay resistance such as multiple toxins and a susceptible refuge. These strategies may also be useful for host-plant resistant crops, but more research is needed on their applicability. We investigated the interaction between a susceptible refuge and an insecticidal seed treatment to manage virulence in the soybean aphid. We tested four scenarios of an insecticidal seed treatment (plus an untreated control) in a microcosm containing 25% aphid-susceptible (refuge) and 75% aphid-resistant soybeans. Independent cohorts of plants were infested every week with avirulent and virulent aphids at equal frequencies. We used a molecular marker to estimate the change in virulence frequency across different plant maturities (from 7 to 42 days after planting). The presence of an insecticidal seed treatment on either the susceptible or resistant soybean decreased the overall population size of the soybean aphid. However, the insecticidal seed treatment impacted both virulent and avirulent aphids similarly, and only altered frequencies in favor of virulence when the sole susceptible plant (i.e., refuge) was treated. Under our experimental conditions, the frequency of avirulent aphids persisted with the use of a refuge. Although an insecticidal seed treatment decreased the overall aphid population size, it did not appear to benefit virulence management. © 2021 Society of Chemical Industry.

Jasmonic Acid-Isoleucine (JA-Ile) Is Involved in the Host-Plant Resistance Mechanism Against the Soybean Aphid (Hemiptera: Aphididae).

Host-plant resistance (HPR) is an important tool for pest management, affording both economic and environmental benefits. The mechanisms of aphid resistance in soybean are not well understood, but likely involve the induction of the jasmonic acid (JA) pathway, and possibly other phytohormone signals involved in plant defense responses. Despite the efficacy of aphid resistance in soybean, virulent aphids have overcome this resistance through mostly unknown mechanisms. Here, we have used metabolomic tools to define the role of plant phytohormones, especially the JA pathway, in regulating interactions between aphid-resistant soybean and virulent aphids. We hypothesized that virulent aphids avoid or suppress the JA pathway to overcome aphid resistance. Our results suggested that aphid-resistant soybean increased accumulation of JA-isoleucine (JA-Ile) only when infested with avirulent aphids; virulent aphids did not cause induction of JA-Ile. Further, applying JA-Ile to aphid-resistant soybean reduced subsequent virulent aphid populations. The concentrations of other phytohormones remained unchanged due to aphid feeding, highlighting the importance of JA-Ile in this interaction. These results increase our knowledge of soybean resistance mechanisms against soybean aphids and contribute to our understanding of aphid virulence mechanisms, which will in turn promote the durability of HPR.

Soybean aphids adapted to host-plant resistance by down regulating putative effectors and up regulating transposable elements

In agricultural systems, crops equipped with host-plant resistance (HPR) have enhanced protection against pests, and are used as a safe and sustainable tool in pest management. In soybean, HPR can control the soybean aphid (Aphis glycines), but certain aphid populations have overcome this resistance (i.e., virulence). The molecular mechanisms underlying aphid virulence to HPR are unknown, but likely involve effector proteins that are secreted by aphids to modulate plant defenses. Another mechanism to facilitate adaptation is through the activity of transposable elements, which can become activated by stress. In this study, we performed RNA sequencing of virulent and avirulent soybean aphids fed susceptible or resistant (Rag1 + Rag2) soybean. Our goal was to better understand the molecular mechanisms underlying soybean aphid virulence. Our data showed that virulent aphids mostly down regulate putative effector genes relative to avirulent aphids, especially when aphids were fed susceptible soybean. Decreased expression of effectors may help evade HPR plant defenses. Virulent aphids also transcriptionally up regulate a diverse set of transposable elements and nearby genes, which is consistent with stress adaptation. Our work demonstrates two mechanisms of pest adaptation to resistance, and identifies effector gene targets for future functional testing.

Soybean aphid (Hemiptera: Aphididae) response to lambda-cyhalothrin varies with its virulence status to aphid-resistant soybean.

Soybean aphid, Aphis glycines, is an invasive insect in North America, considered one of the most important pests of soybean. Their management relies heavily on foliar insecticides, but there is growing effort to expand these tools to include aphid-resistant varieties. We explored if the LC50 and LC25 of lambda-cyhalothrin varied between virulent (resistant to Aphis glycines (Rag) soybeans) and avirulent (susceptible to Rag-genes soybeans) populations of soybean aphid with a leaf-dip bioassay. We also investigated the response to the LC25 of lambda-cyhalothrin on adults (F0) and their progeny (F1) for both avirulent and virulent soybean aphid. The LC50 of the virulent aphid population was significantly higher compared with the LC50 of the avirulent population. The LC25 significantly reduced fecundity of the F0 generation of avirulent soybean aphid, but no significant effect was observed for virulent aphids. In addition, the LC25 significantly shortened the adult pre-oviposition period (APOP) and lengthened the total pre-oviposition period (TPOP) of avirulent aphids, while the mean generation time (T) was significantly increased. For the virulent aphid, sublethal exposure significantly lengthened development time of first and third instars, TPOP, and adult longevity. In addition, all demographic parameters of virulent soybean aphid were significantly affected when they were exposed to the LC25 of lambda-cyhalothrin. Our results demonstrate lambda-cyhalothrin is less toxic to virulent aphids and exposure to the LC25 can trigger hormesis, which may have implications for the long-term management of this pest with this insecticide as well as with aphid-resistant varieties of soybean. © 2019 Society of Chemical Industry.

Weekly Survivorship Curves of Soybean Aphid Biotypes 1 and 4 on Insecticidal Seed-Treated Soybean.

Thiamethoxam, an insecticide used in soybean seed treatments, effectively suppresses soybean aphids (Aphis glycines) Matsumura (Hemiptera: Aphididae) for a short time after planting. However, exactly when and how quickly soybean aphid populations could increase is unknown. Likewise, we lack data on virulent soybean aphid biotypes (that can overcome soybean resistance) when fed on seed-treated soybean. Determining the survival of soybean aphids over time on insecticidal seed-treated soybean is critical for improving soybean aphid management and may provide insights to manage aphid virulence to aphid resistant-soybean. In greenhouse and field experiments, aphid-susceptible soybean plants (with and without an insecticidal seed treatment) were infested at 7, 14, 21, 28, 35, and 42 days after planting (DAP). We compared aphid survival among biotypes 1 (avirulent) and 4 (virulent) and insecticide treatment 72 h after infestation. We also measured thiamethoxam concentrations in plant tissue using liquid chromatography-tandem mass spectrometry. As expected, soybean aphid survival was significantly lower on seed-treated soybean up to 35 DAP for both biotypes, which correlates with the decrease of thiamethoxam in the plant over time. Moreover, we found no significant difference between avirulent and virulent biotype survivorship on insecticidal seed-treated soybean plants, although we did find significantly greater survival for the virulent biotype compared with the avirulent biotype on untreated soybean in the field. In conclusion, our study further characterized the relative short duration of seed treatment effectiveness on soybean aphid and showed that survivorship of virulent aphids on seed-treated soybean is similar to avirulent aphids.

Determining the duration of Aphis glycines (Hemiptera: Aphididae) induced susceptibility effect in soybean

Insect herbivores can increase the suitability of host plants for conspecifics by inducing susceptibility. Induced susceptibility can be separated into feeding facilitation, whereby herbivore feeding increases performance of conspecifics regardless of the genotype of the herbivore or plant, and obviation of resistance, whereby feeding by a virulent herbivore increases performance of avirulent conspecifics on resistant plants. Both forms occur between Aphis glycines (Hemiptera: Aphididae) and soybean. In natural and agricultural settings, A. glycines populations can colonize plants for brief periods before emigrating or being removed due to predation or insecticides. It is unclear if induced susceptibility lasts beyond the period when A. glycines are present on the plant. We measured the duration of induced susceptibility in the A. glycines-soybean system within a growth chamber by removing inducer populations after 24 h. We used an A. glycines-resistant soybean infested with an inducer population of either virulent, avirulent, or no aphids. Response populations of either virulent or avirulent aphids were added at three post-infestation times (24, 120, 216 h) and their densities measured 11 days after infestation. Feeding facilitation was lost within 24 h of the removal of avirulent inducer populations, and obviation of resistance diminished over time and was completely lost within 216 h of the removal of the virulent inducer populations. We discuss how these results support a hypothesis that virulence in A. glycines is due to effector proteins secreted by feeding aphids. We suggest that the duration of induced susceptibility may impact the durability of A. glycines resistance in soybean.

Soybean Aphid (Hemiptera: Aphididae) Response to Soybean Plant Defense: Stress Levels, Tradeoffs, and Cross-Virulence

A variety of management methods to control the soybean aphid (Aphis glycines Matsumura) have been investigated since its invasion into North America in 2000, among them plant resistance has emerged as a viable option for reducing aphid damage to soybeans and preventing outbreaks. Plant resistance methods often use natural soybean plant defenses that impose stress on aphids by reducing fitness and altering behavior. Research efforts have heavily focused on identification and development of aphid resistant soybean varieties, leaving much unknown about soybean aphid response to stressful host plant defenses. In this study, we aimed to 1) evaluate lifetime fitness consequences and phenotypic variation in response to host plant-induced stress and 2) investigate whether trade-offs involving fitness costs and/or cross-virulence to multiple antibiotic soybean varieties exists. We compared aphid survival and reproduction during and after a short period of exposure to soybeans with the Rag2 resistance gene and measured aphid clonal variation in response to Rag2 soybeans. In addition, we measured the performance of Rag2 virulent and avirulent aphids on five soybean varieties with various forms of antibiotic resistance. Our results indicate that plant defenses impose high levels of stress and have long-term fitness consequences, even after aphids are removed from resistant plants. We identified one aphid clone that was able to colonize Rag2 among the seven clones tested, suggesting that virulent genotypes may be prevalent in natural populations. Finally, although we did not find evidence of cross-virulence to multiple antibiotic soybean varieties, our results suggest independent mechanisms of aphid virulence to Rag1 and Rag2 that may involve fitness costs.

Mi-mediated aphid resistance in tomato: tissue localization and impact on the feeding behavior of two potato aphid clones with differing levels of virulence

The Mi-1.2 gene in tomato, Solanum lycopersicum L. (Solanaceae), confers resistance against several herbivores, including the potato aphid, Macrosiphum euphorbiae (Thomas) (Hemiptera: Sternorrhyncha: Aphididae) and the sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Sternorrhyncha: Aleyrodidae). Previous studies on the tissue localization of resistance have given varying results; whitefly resistance was attributed to factors localized in the mesophyll or epidermis, whereas aphid resistance was attributed to factors localized in the phloem. Our study utilizes the direct current electrical penetration graph (DC-EPG) technique to compare aphid feeding behavior on resistant (Mi-1.2+) and susceptible (Mi-1.2-) tomato plants. This study also compares the impact of resistance on the feeding behavior of two aphid clones that vary in their virulence, or their ability to survive and reproduce on resistant plants. Previous work had shown that the avirulent WU11 clone is almost completely inhibited by resistance, whereas the semi-virulent WU12 clone can colonize resistant hosts. Here, DC-EPG analysis shows that both aphid clones take longer to initiate cell sampling and to establish a confirmed sieve element phase on resistant plants than on susceptible hosts, and have shorter ingestion periods on resistant plants. However, the magnitude of these deterrent effects is far less for the semi-virulent clone than for the avirulent aphids. In particular, the WU12 clone is less sensitive to factors that limit sieve element ingestion, showing shorter non-probe duration and rapidly establishing sustained phloem ingestion on resistant plants when compared to the WU11 clone. We conclude that, in addition to previously described factors in the phloem that inhibit ingestion, Mi-mediated aphid resistance also involves factors (possibly in the mesophyll and/or epidermis) that delay initiation of phloem salivation, and that act in the intercellular spaces to deter the first cell sampling. Furthermore, the relative effectiveness of these components of resistance differs among insect populations.

Tritrophic interactions among Macrosiphum euphorbiae aphids, their host plants and endosymbionts: Investigation by a proteomic approach

The Mi-1.2 gene in tomato confers resistance against certain clones of the potato aphid ( Macrosiphum euphorbiae). This study used 2D-DIGE coupled with protein identification by MALDI-TOF-MS to compare the proteome patterns of avirulent and semivirulent potato aphids and their bacterial endosymbionts on resistant ( Mi-1.2+) and susceptible ( Mi-1.2−) tomato lines. Avirulent aphids had low survival on resistant plants, whereas the semivirulent clone could colonize these plants. Eighty-two protein spots showed significant quantitative differences among the four treatment groups, and of these, 48 could be assigned putative identities. Numerous structural proteins and enzymes associated with primary metabolism were more abundant in the semivirulent than in the avirulent aphid clone. Several proteins were also up-regulated in semivirulent aphids when they were transferred from susceptible to resistant plants. Nearly 25% of the differentially regulated proteins originated from aphid endosymbionts and not the aphid itself. Six were assigned to the primary endosymbiont Buchnera aphidicola, and 5 appeared to be derived from a Rickettsia-like secondary symbiont. These results indicate that symbiont expression patterns differ between aphid clones with differing levels of virulence, and are influenced by the aphids’ host plant. Potentially, symbionts may contribute to differential adaptation of aphids to host plant resistance.

Modelling the population dynamics of different aphid genotypes in plant variety mixtures

Mathematical models demonstrate that intermixing plants of a susceptible variety among resistant plants within a field may reduce the rate at which resistance-adapted (virulent) aphid genotypes develop. This process should occur if the initial proportion of the virulent aphids is small, if the aphids randomly immigrate to fields, and if their population is subsequently depressed by insecticide application or natural enemies. In these conditions the avirulent aphids will usually reach the field first providing conditions for an increase in mortality factors which then suppress later arriving virulent aphids. The effects of various factors on the magnitude of this result were found using two different modelling approaches. Each approach involved a within season ecological model in which aphids reproduced parthenogenetically and a between season one locus genetic model in which the allele for virulence was assumed to be either dominant or recessive. The first approach, using deterministic Lotka-Volterra equations, demonstrated that if the initial proportion of virulence was below a critical value, virulence would quickly be eliminated from the population even if the avirulent aphids had no selective advantage. The critical value was determined by the proportion of susceptible plants, the level of resistance, the probability of aphids entering the field, the aphid population growth rate, the time when mortality factors appeared, and the cost of virulence. The second approach expanded on the previous model by introducing stochastic effects, using more realistic population growth equations, and following spatial and movement patterns of the organisms. The general conclusion from the stochastic model was similar to that of the deterministic model, with the additional result that most parameters did not greatly effect the outcome. The most important parameters were the percent susceptible plants in the field, the level of resistance, and the aphid population growth rate. In the genetic section of both models the type of inheritance of virulence made only small differences in these results if the initial proportion of the virulent phenotype was the same.