Potential for biotic interference of a classical biological control agent of the soybean aphid

The degree to which resident biota can inhibit the ability of an introduced biological control agent to establish and be effective is termed biotic interference. Studying biotic interference prior to a release using the actual agent is logistically difficult, however, due to quarantine restrictions. An alternative solution is to study biotic interference against a surrogate species in the intended range of introduction, with the expectation that biotic interference against the actual agent will be similar. This study assessed how biotic interference, mostly by generalist predators, may affect establishment of classical biological control agents of the soybean aphid, Aphis glycines Matsumura, in North America. The parasitoid Aphidius colemani Viereck was used as a surrogate for Asian aphidiine braconids such as Binodoxys communis (Gahan). We conducted a factorial field experiment that measured the effect of releasing A. colemani and of excluding resident natural enemies using field cages on soybean aphid populations. We also conducted molecular gut-contents analyses on predators collected in release plots to determine which species fed upon A. colemani. Releasing A. colemani in open field plots increased soybean aphid control beyond that observed in open field plots alone, despite indications that intraguild predation of A. colemani occurred. Thus, biotic interference was not sufficient to eliminate the contribution of A. colemani on soybean aphid suppression during the course of our experiment. Molecular gut-contents analysis revealed that at least two predators, Harmonia axyridis (Pallas) and Chrysoperla carnea Stephens, engaged in intraguild predation against A. colemani. The prolonged effect of intraguild predation on parasitoid establishment remains to be determined.     

Seasonal abundance of resident parasitoids and predatory flies and corresponding soybean aphid densities, with comments on classical biological control of soybean aphid in the Midwest

Seasonal abundance of resident parasitoids and predatory flies, and corresponding soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), densities were assessed in soybean fields from 2003 to 2006 at two locations in lower Michigan. Six parasitoid and nine predatory fly species were detected in 4 yr by using potted plants infested with soybean aphid placed in soybean fields. The parasitoid Lysiphlebus testaceipes Cresson (Hymenoptera: Braconidae) and the predatory flies Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae), and Allograpta obliqua Say (Diptera: Syrphidae) were most numerous. Generally, L. testaceipes was more abundant late in the soybean growing season, but it also occurred during soybean vegetative growth; A. obliqua was more abundant during vegetative growth; and A. aphidimyza was common throughout the season. Soybean plants were visually inspected to estimate densities of soybean aphid, mummified aphids, and immature predatory flies. From 2003 to 2006, parasitism rates were inversely correlated with aphid density: percentage of parasitism was always very low (< or = 0.1%) at high aphid densities (> 100 aphids per plant), and higher parasitism, up to 17%, was observed at very low aphid densities (< 1 aphid per plant). Populations of immature predatory flies, particularly A. aphidimyza, generally increased in soybean fields with increasing soybean aphid populations, but aphids always outnumbered immature flies by 100-21,000-fold when flies were detected. Rearing field-collected aphid in 2006 substantiated that parasitism varied widely, with parasitism in most cases < 10%. Based on findings of low parasitism and predation, positive response to changing aphid densities by predatory flies but not parasitoids, early season abundance primarily of predatory flies, and past findings on these taxa's diversity and abundance, we discuss the potential use of exotic parasitoids and predatory flies to enhance soybean aphid biological control.     

大豆蚜的生物学防治技术

大豆蚜AphisglycinesMatsumura是亚洲大豆种植区的一种主要农业害虫。近年来,大豆蚜又先后侵入北美洲和大洋州等地,对当地的大豆生产构成了潜在威胁,正成为一种世界性的农业害虫。文章对大豆蚜的分布、危害、生物学特征、天敌和防治技术等方面的研究现状进行了详细论述。     

Compatibility of aphid resistance in soybean and biological control by the parasitoid Aphidius colemani (Hymenoptera: Braconidae)

Biological control and soybean cultivars bred for increased resistance to the soybean aphid (Aphis glycines) are two approaches used to manage this serious pest of soybeans in North America. However, as with many other pest systems, the compatibility of these two pest management approaches has not been studied in detail. The aphidiine wasp Aphidius colemani is one of several candidate species for biological control of the soybean aphid in soybean in North America. Resistance to the soybean aphid in the USDA soybean cultivar Dowling is largely controlled by a single dominant gene Rag1, which is the focus of plant breeding programs directed against the soybean aphid. In this study, we measured developmental and behavioral differences in the parasitic wasp A. colemani when it attacked soybean aphids feeding on either the aphid-resistant Dowling or aphid-susceptible Glenwood cultivars of soybean. We used a combination of choice and no-choice experiments to examine the effects of host plant cultivar on the number of parasitized aphids formed and the sex ratio and body weights of adult offspring produced. Significantly more aphids were parasitized when they fed on Glenwood compared to Dowling and these offspring were larger when they developed in aphids that fed on Glenwood soybeans. To distinguish between effects on foraging decisions and offspring survivorship, we conducted an additional experiment that followed the oviposition decisions and fate of each parasitized aphid. Foraging female A. colemani spent less time handling individual aphids and encountered and attacked aphids at a higher rate when they fed on aphids feeding on Glenwood soybeans than aphids feeding on Dowling soybeans. Furthermore, wasp survivorship in aphids was greater on Glenwood than Dowling. Taken together, aphid-resistance in soybeans has negative effects on foraging behavior and offspring fitness of A. colemani raising concerns about the compatibility of these two pest management approaches.     

Temporal variability of aphid biological control in contrasting landscape contexts

Landscape complexity may provide ecosystem services to agriculture through the provision of natural enemies of agricultural pests. Strong positive effect of adjacent semi-natural habitats on natural enemies in croplands has been evidenced, but the resulting impact on biological control remains unclear. Taking into account the temporal dynamics of pest and natural enemies in agricultural landscapes provides better resolution to the studies and better understanding of the biological control service.In this study, the population dynamics of aphids and two groups of predators (coccinellid and carabid beetles) were examined. Insects were sampled in 20 wheat fields, surrounded by structurally simple and complex landscapes in Chilean central valley. Considering the whole sampling period, the diversity of aphids and natural enemies were similar in wheat crops surrounded by both types of landscapes, and the abundance of ladybirds was higher in crops in the complex landscapes. The dynamics of predators was more advanced in complex landscapes than in the simple ones, whereas the dynamics of aphids were similar in both types of landscape. Negative correlation between abundance of predators and aphid population growth rate in both landscape contexts were observed suggesting a control of the pest population by the predators. Different temporal patterns were observed in these correlations in the two landscape contexts, which suggests differences in the biological control related to the landscape composition.The present study shows that colonization of crops by natural enemies occurs sooner in structurally complex landscapes and suggests that this early colonization may facilitate an early and efficient control of aphid populations, nevertheless the biological control efficiency seems to be higher in structurally simple landscapes later in the season.     

Alfalfa cyclitols in the honeydew of an aphid

The free cyclitols pinitol, ononitol and myo-inositol occur in the honeydew (excreta) of pea aphids (Acyrthosiphon pisum) which feed on pea aphid-susceptible alfalfa (Medicago sativa cv Caliverde). These cyclitols also occur in the leaves and stems of alfalfa. Aphids were incapable of de novo synthesis of these cyclitols. Honeydew production by the pea aphid results from ingesting phloem-sap, so the occurrence of cyclitols in honeydew results from their translocation in the phloem. The relatively high content of myo-inositol in honeydew indicates that it is selectively translocated. The most abundant alfalfa cyclitol, pinitol, had no effect on aphid feeding behavior at concentrations up to 1% (w/v; artificial diet).     

Parasitism of soybean aphid by Aphelinus species on soybean susceptible versus resistant to the aphid

The soybean aphid, Aphis glycines, is native to Asia, but during the last decade it has invaded North America, where it has spread to most soybean growing regions and become the most important insect pest of soybean. Current control of soybean aphid relies primarily on insecticides, but alternatives to insecticidal control are being explored, especially host plant resistance and biological control, which may interact positively or negatively. Research on host plant resistance to the soybean aphid has revealed six genes that affect resistance. We measured the impact of the two most studied resistance loci, Rag1 and Rag2, on two parasitoid species: Aphelinus glycinis, a recently described species from Asia, which is being introduced into the USA to control the soybean aphid, and Aphelinus certus, also from Asia but accidentally introduced into the USA. Resistance did not affect oviposition by either parasitoid species. However, resistance did reduce successful parasitism by A. glycinis, with each resistance allele causing a two-fold reduction in number of mummified aphids. The resistance alleles did not affect adult emergence, sex ratio, or the size of A. glycinis. For A. certus, the Rag1 resistance allele had no effect on parasitism, while the Rag2 resistance allele reduced parasitism four-fold. On the other hand, the Rag1 resistance allele increased the frequency of males among progeny and decreased female size of A. certus. Despite the reduction in parasitism, these parasitoids are nonetheless able to parasitize the soybean aphid on resistant soybean, which means that they should still contribute to the management of soybean aphid on resistant varieties.     

Antagonistic effects of soybean viruses on soybean aphid performance

Although there is long-standing recognition that pest complexes require different management approaches than individual pests, relatively little research has explored how pests interact. In particular, little is known of how herbivorous insects and plant pathogens interact when sharing the same host plant. The soybean aphid, Aphis glycines Mastumura, a recently introduced pest of soybean in the upper midwestern United States, and a complex of plant viruses vectored to soybean by insects have become a major concern for growers in the region. Given the abundance of soybean aphid and the increase in virus incidence in recent years, soybean aphids often use soybean infected by plant viral pathogens. We tested the hypothesis that soybean aphid performance is affected by virus infection of soybean plants. We conducted a series of field and laboratory experiments that examined how infection of soybeans with the common plant viruses, alfalfa mosaic, soybean mosaic, and bean pod mottle viruses, influenced soybean aphid performance. Soybean plants (in the field and laboratory) were hand inoculated with individual viruses, and aphids were allowed to colonize plants naturally in field experiments or added to the plants in clip-cages or within mesh bags in laboratory assays. In the field, aphid density on uninfected control soybean plants was nearly double that on infected plants. In laboratory assays, aphid population growth rates were on average 20% lower for aphids on virus infected compared with uninfected plants. Life table analyses showed that increased mortality on virus-infected plants likely explain differences in aphid population growth. Although there was some heterogeneity in the significance of treatment effects among different experiments, when independent experiments are taken together, there is on average an overall negative effect of these viruses on soybean aphids.     

Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America

In summer 2007, the Asian parasitoid Binodoxys communis (Hymenoptera: Braconidae) was released in North America for control of the exotic soybean aphid, Aphis glycines (Hemiptera: Aphididae). Despite its comparatively narrow host range, releases of B. communis may still constitute a risk to native aphid species. To estimate the risk of exposure of non-target aphids to B. communis, we merged assessments of temporal co-occurrence with projections of spatial overlap between B. communis and three native aphid species, and in-field measurements of the incidence of ecological filters that may protect these aphids from parasitism. Temporal co-occurrence was assessed between A. glycines and native aphids (Aphis asclepiadis, Aphis oestlundi, and Aphis monardae) at four different locations in Minnesota, USA. The degree of temporal overlap depended greatly on location and aphid species, ranging between 0 and 100%. All of the native aphids were tended by multiple species of ants, with overall ant-attendance ranging from 26.1 to 89.6%. During temporal overlap with A. glycines, 53 ± 11% of A. monardae colonies were partly found in flower heads of their host plant, with flowers acting as a physical refuge for this aphid. The extent of geographic overlap between B. communis and native aphids based upon Climex modeling was 17–28% for A. monardae, 13–22% for A. oestlundi, 46–55% for A. asclepiadis and 12–24% for the A. asclepiadis species complex. The estimated overall probability of potential exposure of B. communis on native aphids was relatively low (P = 0.115) for A. oestlundi and high (P = 0.550) for A. asclepiades. Physical and ant-mediated refuges considerably lowered probability of population-level impact on A. monardae, and could lead to substantial reduction of exposure for the other native aphids. These findings are used to make broader statements regarding the ecological safety of current B. communis releases and their potential impact on native aphid species in North America.     

Inheritance of soybean aphid resistance in 21 soybean plant introductions

Key Message

The Rag2 region was frequently identified among 21 F ₂ populations evaluated for soybean aphid resistance, and dominant gene action and single-gene resistance were also commonly identified.

Abstract

The soybean aphid [Aphis glycines Matsumura (Hemiptera: Aphididae)] is one of the most important insect pests of soybean [Glycine max (L.) Merr] in the northern USA and southern Canada, and four resistance loci (Rag1–rag4) have been discovered since the pest was identified in the USA in 2000. The objective of this research was to determine whether resistance expression in recently identified soybean aphid-resistant plant introductions (PIs) was associated with the four Rag loci using a collection of 21 F₂ populations. The F₂ populations were phenotyped with soybean aphid biotype 1, which is avirulent on plants having any of the currently identified Rag genes, using choice tests in the greenhouse and were tested with genetic markers linked to the four Rag loci. The phenotyping results indicate that soybean aphid resistance is controlled by a single dominant gene in 14 PIs, by two genes in three PIs, and four PIs had no clear Mendelian inheritance patterns. Genetic markers flanking Rag2 were significantly associated with aphid resistance in 20 PIs, the Rag1 region was significantly identified in five PIs, and the Rag3 region was identified in one PI. These results show that single dominant gene action at the Rag2 region may be a major source for aphid resistance in the USDA soybean germplasm collection.     

Enhancing biological control by an omnivorous lacewing: Floral resources reduce aphid numbers at low aphid densities

The availability of plant resources to omnivorous arthropod predators may have a positive, negative or negligible effect on their population densities and predation rates, depending on the availability of prey. At high prey densities, flowering buckwheat has been shown to negatively impact populations of the brown lacewing, an omnivorous predator, due to the probable increase in parasitism rate of lacewing larvae by their primary parasitoid, Anacharis zealandica. However, little is known about the effect of buckwheat flowers on this insect community at low prey densities. We used field cages to assess the effects of nectar provision by flowering buckwheat on the population dynamics of the pea aphid, the brown lacewing and its parasitoid A. zealandica in an alfalfa field, under low aphid densities in the New Zealand summer. The insects were sampled every 2 weeks with a suction device, then counted and released on each sampling date from 15 January to 15 March 2007. Buckwheat significantly increased lacewing populations and significantly decreased aphid numbers by 70% and 39%, respectively. The buckwheat had its greatest effect at the end of summer (February/March) for both these species. It had no effect on A. zealandica abundance.     

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.     

Potential for augmentative biological control of black bean aphid in California sugarbeet

In northern California, black bean aphid (Aphis fabae Scopoli complex) can be a major pest of sugarbeet, particularly in spring-planted fields. The major natural enemies of the aphid are predators, including the coccinellidsHippodamia convergens Guerin,Coccinella novemnotata Herbst &C. septempunctata L., and the chrysopidsChrysopa oculata Say &C. nigricornis Burmeister. Augmentative releases of eggs of eitherChrysoperla carnea (Stephens) orC. rufilabris (Burmeister) failed to significantly reduce aphid populations under field conditions. This was attributed in part to incompatibility between black bean aphids and lacewing larvae from commercial sources. Application of food sprays containing yeast hydrolysate, sucrose and molasses resulted in increased densities of eggs and adults ofC. carnea in treated plots. These results suggest that the potential for augmentative biological control of black bean aphid through the application of food sprays is greater than that for release of commercially available lacewings. Regardless of method, an holistic approach to augmentation that takes into account the ecological structure of the target agroecosystem will be required. Some aspects of “pre-emptive” biological control are discussed.     

Lack of strong refuges allows top-down control of soybean aphid by generalist natural enemies

Refuges have been shown to be important mediators of predator–prey interactions, and in particular, have been proposed as a potential mechanism allowing herbivore populations to reach outbreak levels. However, very little research on the role of refuges has been conducted in systems dominated by generalist predators. We investigated the existence of refuges from predation for the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) at multiple scales. This species invaded North America and in spite of previous studies demonstrating strong suppression by generalist natural enemies, its populations periodically cause significant economic losses. Using naturally occurring populations of soybean aphid and its natural enemies, we tested for the presence of A. glycines spatial and dynamic refuges at the within-field, single plant, and within-plant scale. At the within-field level, we found only weak and transient spatial patterns in aphid populations suggesting the lack of spatial refuges at this scale. Similarly, at the plant level we found no individual colonies that escaped predation and aphid suppression was 9- to 28-fold greater in comparison with caged controls regardless of initial aphid density. When high aphid populations were exposed to predation they were rapidly reduced to levels close to the average field density and showed reduced per capita growth rates, indicating an absence of dilution of predation risk at increased aphid density. Finally, we found a significant shift in the distribution of aphids to the lower portions of the plant in the presence of generalist predators, suggesting a partial refuge from predation at the within-plant scale. Overall, we found the naturally occurring community of generalist predators to exert strong top-down suppression of soybean aphid populations at multiple scales, and no evidence that the presence of refuges at the scales studied can lead to outbreak populations. The partial refuge from predation at the within-plant scale revealed in our study may have important consequences for the within-season population dynamics of A. glycines, since it may be associated with low plant quality tradeoffs, and therefore warrants further research.     

Relationships between soybean shoot nitrogen components and soybean aphid populations

Defining the relationships between soybean (Glycine max [L.] merr.) shoot nitrogen (N) components and soybean aphid (Aphis glycines Matsumura) populations will increase understanding of the biology of this important insect pest. In this 2-year field study, caged soybean plants were infested with soybean aphids (initial infestation of 0, 10, 50, or 100 aphids plant^?1) at the fifth node developmental stage. Soybean aphid populations, soybean shoot dry weight, and shoot concentrations of nitrate-N, ureide-N, and total N were measured starting at full bloom through full seed soybean development stages. Soybean aphid population as well as shoot concentration of ureide-N increased rapidly starting at full bloom, peaked at beginning seed, and dramatically decreased by full seed soybean reproductive stages. Regression analysis indicated significant relationships (P = 0.01; r = 0.71) between soybean aphid populations and shoot ureide-N concentration. Thus, soybean aphid population levels appear to coincide with shoot ureide-N concentrations in the soybean plant.     

Determining the optimal timing of foliar insecticide applications for control of soybean aphid (Hemiptera: Aphididae) on soybean

Field experiments were performed over 3 yr to examine the impact of insecticide application timing to control soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), populations and to prevent soybean yield losses. Experiments were conducted in early and late-planted soybean, Glycine max (L.) Merr. Insecticide applications were made based on soybean growth stages. In 2001, applications were made at V1, V3, R2, and R3 growth stages; in 2002 and 2003, applications were made at R2, R3, and R4 stages. Additional treatments consisted of an unsprayed control and a multiple spray treatment that received insecticide applications at 7-10-d intervals. Soybean aphid densities were recorded throughout the growing season, and yields were measured. Soybean aphid populations varied considerably across years and planting dates. In general, late-planted soybean exhibited higher aphid pressure than early planted soybean, and experiments in 2002 had lower aphid numbers than those in 2001 and 2003. The multiple spray treatment significantly increased yield over the control in four of the six experiments, the exceptions being 2002 late planted and 2003 early planted. This suggests that soybean aphid populations were not large enough to cause yield losses in these two experiments. The R3 spray treatment increased yield in three of the six experiments (2001 late planting, 2002 early planting, and 2003 late planting), the R2 spray treatment increased yield in two of six experiments (2001 and 2003 late plantings), and the V1 application increased yield over the control in the 2001 late-planted experiment. Results suggest that when aphid populations are high insecticide applications made at R2 and R3 plant stages are most effective in preventing yield loss.     

Soil potassium deficiency affects soybean phloem nitrogen and soybean aphid populations

The soybean aphid is an invasive pest in the midwest United States, with frequent population outbreaks. Previous work has shown that aphid population densities are higher on potassium-deficient soybean than on healthy soybean. The experiments reported here test the hypotheses that the potassium nutrition of the host plant affects the forms of phloem nitrogen available to soybean aphids, and subsequently, their abundance. In field surveys and an exclusion cage study when aphid populations were high, soybean plants with potassium deficiency symptoms had a higher density of soybean aphids than plants without deficiency symptoms. In clip cage experiments, this effect was caused by earlier aphid reproduction and higher numbers of aphid nymphs per mother on plants growing in lower-potassium soil. In phloem exudation samples, the percentage of asparagine, an important amino acid for aphid nutrition, increased with decreasing soil potassium, perhaps because of potassium's role in the nitrogen use of the plant. Taken together, these results show that soybean potassium deficiency can lead to higher populations of soybean aphid through a bottom-up effect. A possible mechanism for this relationship is that soybean potassium deficiency improves the nitrogen nutrition of these N-limited insects. By releasing these herbivores from N limitation, host plant potassium deficiency may allow soybean aphid populations to reach higher levels more rapidly in the field.     

Fine mapping the soybean aphid resistance gene Rag1 in soybean

The soybean aphid (Aphis glycines Matsumura) is an important soybean [Glycine max (L.) Merr.] pest in North America. The dominant aphid resistance gene Rag1 was previously mapped from the cultivar ‘Dowling’ to a 12 cM marker interval on soybean chromosome 7 (formerly linkage group M). The development of additional genetic markers mapping closer to Rag1 was needed to accurately position the gene to improve the effectiveness of marker-assisted selection (MAS) and to eventually clone it. The objectives of this study were to identify single nucleotide polymorphisms (SNPs) near Rag1 and to position these SNPs relative to Rag1. To generate a fine map of the Rag1 interval, 824 BC₄F₂ and 1,000 BC₄F₃ plants segregating for the gene were screened with markers flanking Rag1. Plants with recombination events close to the gene were tested with SNPs identified in previous studies along with new SNPs identified from the preliminary Williams 82 draft soybean genome shotgun sequence using direct re-sequencing and gene-scanning melt-curve analysis. Progeny of these recombinant plants were evaluated for aphid resistance. These efforts resulted in the mapping of Rag1 between the two SNP markers 46169.7 and 21A, which corresponds to a physical distance on the Williams 82 8× draft assembly (Glyma1.01) of 115 kilobase pair (kb). Several candidate genes for Rag1 are present within the 115-kb interval. The markers identified in this study that are closely linked to Rag1 will be a useful resource in MAS for this important aphid resistance gene.     

A novel locus for soybean aphid resistance

The soybean aphid (Aphis glycines Matsumura) is an important pest on soybean [Glycine max (L.) Merr.] in North America. Aphid resistance has recently been found on plant introduction (PI) 567543C, but little is known about its genetic control. The objectives of this study were to identify the resistance genes in PI 567543C with molecular markers and validate them in a different genetic background. A mapping population of 249 F₄ derived lines from a cross between PI 567543C and a susceptible parent was investigated for aphid resistance in both the greenhouse and the field. The broad sense heritability of aphid resistance in the field trial was over 0.95. The segregation of aphid resistance in this population suggests a major gene controlling the resistance. Bulked segregant analysis with molecular markers revealed a potential genomic region. After saturating this putative region with more markers, a genetic locus was mapped in an interval between Sat_339 and Satt414 on chromosome 16 (linkage group J) using the composite interval mapping method. This locus explained the majority of the phenotypic variation ranging from 84.7% in the field trial to 90.4% in the greenhouse trial. Therefore, the aphid resistance in PI 567543C could be mainly controlled by this gene. This aphid resistance gene was mapped on a different chromosome than the other resistance genes reported previously from other resistant germplasms. This gene appears to be additive based on the aphid resistance of the heterozygous lines at this locus. Thus, a new symbol Rag3 is used to designate this gene. Moreover, Rag3 was confirmed in a validation population. This new aphid-resistance gene could be valuable in breeding aphid resistant cultivars.