Soybean Aphid Research Articles

Transcriptional responses of soybean aphids to sublethal insecticide exposure

Insecticides are a key tool in the management of many insect pests of agriculture, including soybean aphids. The selection imposed by insecticide use has often lead to the evolution of resistance by the target pest through enhanced detoxification mechanisms. We hypothesised that exposure of insecticide-susceptible aphids to sublethal doses of insecticides would result in the up-regulation of genes involved in detoxification of insecticides, revealing the genes upon which selection might act in the field. We used the soybean aphid biotype 1 reference genome, version 6.0 as a reference to analyze RNA-Seq data. We identified multiple genes with potential detoxification roles that were up-regulated 12 h after sublethal exposure to esfenvalerate or thiamethoxam. However, these genes were part of a dramatic burst of differential gene expression in which thousands of genes were up- or down-regulated, rather than a defined response to insecticides. Interestingly, the transcriptional burst observed at 12 h s declined dramatically by 24-hrs post-exposure, suggesting a general stress response that may become fine-tuned over time.

Evaluating Soybean Aphid-Resistant Varieties in Different Environments to Estimate Financial Outcomes.

Farmers face many choices when selecting seed for soybean (Glycine max (L.) Merr.) production, including highly desired herbicide tolerance traits. Despite the convenience of herbicide tolerance, resistant weeds and technology fees may reduce utility and profitability of these varieties, especially when commodity prices are low. Sporadic outbreaks of soybean aphid (Aphis glycines Matsumura, Hemiptera: Aphididae) that require insecticide use for optimal yield can be a further complication for farmers in Iowa. Soybean aphid-resistant varieties are commercially available, but in limited genetic backgrounds without herbicide tolerance. We hypothesized yield and value of resistance traits will vary based on the environment. We established plots at two locations with different risks of soybean aphid outbreaks and used two planting dates at each location to mimic different yield environments. In 2016 and 2017, we planted four varieties that varied in their susceptibility to soybean aphids and glyphosate, and applied insecticides if aphid populations reached an economic threshold. Regardless of genetic background, aphid-resistant varieties prevented populations from reaching the economic threshold at all environments. We observed no significant difference in yield between resistant and susceptible varieties, revealing this trait is as effective at protecting yield as an insecticide application on susceptible varieties at the high-risk location. We also explored the value of each variety in different environments. Resistant varieties produced greater potential net revenue than susceptible varieties at the high-risk location, while the opposite occurred at the low-risk location. Resistant varieties with herbicide tolerance, if made available, would be the most valuable across all environments.

Baseline susceptibility to afidopyropen of soybean aphid (Hemiptera: Aphididae) from the north central United States

Afidopyropen, a novel Group 9D insecticide, has proven effective for management of soybean aphid, Aphis glycines (Hemiptera: Aphididae). However, to ensure continued efficacy of this insecticide, insecticide resistance management programs are needed. The goal of this study was to evaluate baseline susceptibility of several populations of soybean aphid to afidopyropen using leaf-dip bioassays in 2017 and 2018. Overall, mortality of adult soybean aphid varied among populations. Lethal concentrations necessary to kill 50% of a population (LC50) for adults ranged from 0.0013 to 0.40 mg a.i. per liter of afidopyropen. Lethal concentrations necessary to kill 70% of a population (LC70) of adults ranged from 0.136 to 13.1 mg a.i. per liter of afidopyropen. Afidopyropen was effective against populations resistant to pyrethroid insecticides, suggesting a lack of cross-resistance between afidopyropen and pyrethroids. Furthermore, afidopyropen was effective against nymphs of soybean aphid with concentrations ranging from 0.0285 to 54.45 mg a.i. per liter of afidopyropen causing 100% mortality by 6 days after exposure. The results reported here can be used for establishment of programs to monitor for development of resistance to this insecticide by soybean aphid.

Comparative Analysis of Intra- and Inter-Specific Genomic Variability in the Peach Potato Aphid, Myzus persicae.

The availability of genomic data in the last decade relating to different aphid species has allowed the analysis of the genomic variability occurring among such species, whereas intra-specific variability has hitherto very largely been neglected. In order to analyse the intra-genomic variability in the peach potato aphid, Myzus persicae, comparative analyses were performed revealing several clone-specific gene duplications, together with numerous deletions/rearrangements. Our comparative approach also allowed us to evaluate the synteny existing between the two M. persicae clones tested and between the peach potato aphid and the pea aphid, Acyrthosiphon pisum. Even if part of the observed rearrangements are related to a low quality of some assembled contigs and/or to the high number of contigs present in these aphid genomes, our evidence reveals that aphid clones are genetically more different than expected. These results suggest that the choice of performing genomes sequencing combining different biotypes/populations, as revealed in the case of the soybean aphid, Aphis glycines, is unlikely to be very informative in aphids. Interestingly, it is possible that the holocentric nature of aphid chromosomes favours genome rearrangements that can be successively inherited transgenerationally via the aphid’s apomictic (parthenogenetic) mode of reproduction. Lastly, we evaluated the structure of the cluster of genes coding for the five histones (H1, H2A, H2B, H3 and H4) in order to better understand the quality of the two M. persicae genomes and thereby to improve our knowledge of this functionally important gene family.

Molecular Basis of Soybean Resistance to Soybean Aphids and Soybean Cyst Nematodes.

Soybean aphid (SBA; Aphis glycines Matsumura) and soybean cyst nematode (SCN; Heterodera glycines Ichninohe) are major pests of the soybean (Glycine max [L.] Merr.). Substantial progress has been made in identifying the genetic basis of limiting these pests in both model and non-model plant systems. Classical linkage mapping and genome-wide association studies (GWAS) have identified major and minor quantitative trait loci (QTLs) in soybean. Studies on interactions of SBA and SCN effectors with host proteins have identified molecular cues in various signaling pathways, including those involved in plant disease resistance and phytohormone regulations. In this paper, we review the molecular basis of soybean resistance to SBA and SCN, and we provide a synthesis of recent studies of soybean QTLs/genes that could mitigate the effects of virulent SBA and SCN populations. We also review relevant studies of aphid–nematode interactions, particularly in the soybean–SBA–SCN system.

Effects of aphid-resistant soybean on nontarget herbivores in Minnesota

The use of aphid-resistant soybean varieties containing Rag genes can provide an effective pest management strategy against soybean aphid (Aphis glycines Matsumura). However, the compatibility between soybean containing Rag genes and the management of other potential soybean pests (i.e., nontarget herbivores) is poorly understood. Therefore, our goal was to (1) assess the efficacy of pyramided (Rag1+Rag2) aphid-resistant soybean for reduction of soybean aphid populations, and (2) determine if aphid-resistant soybean affects populations of nontarget herbivores under field conditions. To accomplish these goals, field experiments were conducted in southeast Minnesota from 2015 to 2017 for a total of five site-years using whole-plant counts to assess soybean aphid densities and sweep-net sampling to estimate nontarget herbivore densities in plots of near-isoline soybean with Rag1+Rag2 (i.e., resistant) or no Rag genes (i.e., susceptible). Plant genotype (i.e., resistant or susceptible) affected seasonal abundance of soybean aphid, with fewer soybean aphids on aphid-resistant than susceptible soybean. Furthermore, plant genotype affected seasonal abundance of bean leaf beetle (Cerotoma trifurcata Forster), green cloverworm (Hypena scabra Fabricius), and potato leafhopper (Empoasca fabae Harris). Aphid-resistant soybean was associated with increased seasonal abundance of bean leaf beetle and reduced seasonal abundance of potato leafhopper and green cloverworm. The abundance of these herbivores was also associated with seasonal abundance of soybean aphid as a covariate. Results presented here confirm the efficacy of aphid-resistant soybean with Rag1+Rag2 against soybean aphid and show that aphid-resistant soybean can influence the seasonal abundance of nontarget herbivores in soybean. However, the magnitude of impacts of aphid-resistant soybean on nontarget herbivores was relatively small and likely of little-to-no agronomic significance, which suggests compatibility of aphid-resistant soybean with management of other potential pests.

Analysis of the extent of synteny and conservation in the gene order in aphids: A first glimpse from the Aphis glycines genome

In the last decade several insect genomes have been sequenced, but for most the chromosomal mapping of the identified scaffolds/annotated genes is not available. The lack of this information makes it difficult to analyse various genetic aspects, including the presence of genome rearrangements and the extent of synteny within and across species. We mapped five multigenic DNA families (major and minor rDNAs, histone gene cluster, esterases and carotenoid desaturases) and seven scaffolds corresponding to 9 Mb of the soybean aphid, Aphis glycines, genome and identified loci spanning the four soybean aphid chromosomes. A comparative analysis of the localization of the annotated A. glycines genes with respect to the peach potato aphid, Myzus persicae, and the fly, Drosophila melanogaster, evidenced a lower degree of synteny between the two aphid species than in the aphid-fly comparison. Only 1.4 genes per syntenic block were observed in aphids in contrast to 2.3 genes per block in flies. This higher chromosomal rearrangement rate in aphids could be explained considering that they possess holocentric chromosomes that can favour the stabilization and inheritance of chromosomal rearrangements. Lastly, our experiments did not detect the presence of chimeric assemblies in the newly available A. glycines biotype 1 genome, differently from what reported in assembled genome of other aphid species, suggesting that chromosomal mapping can be used to ascertain the quality of assembled genomes.

Spray method application of transdermal dsRNA delivery system for efficient gene silencing and pest control on soybean aphid Aphis glycines

RNA interference (RNAi) has been recognized as a novel and safe strategy in pest management due to its high sequence-dependent specificity. However, the existing dsRNA delivery methods largely restrict the application of the RNAi-based pest management strategy; thus, we previously constructed a nanocarrier-based transdermal dsRNA delivery system on the soybean aphid Aphis glycines with the help of nanocarrier and detergent. In the current study, we improved our transdermal dsRNA delivery system with a smaller and cheaper nanocarrier to investigate the efficacy of spraying aphid-infested soybean seedlings to apply our RNA pesticide. A dsRNA/nanocarrier/detergent formulation was performed, and the dsRNA could penetrate the aphid body wall within 4 h with the help of nanocarrier through the topical application. Four potential RNAi target genes (TREH, ATPD, ATPE and CHS1) were selected and cloned, and their dsRNA fragments were synthesized and tested through the transdermal dsRNA delivery system. The delivered dsRNA efficiently silenced the target gene expression with the knockdown effects ranging from 86.86 to 58.87% and resulted in a high mortality up to 81.67% (dsATPD + dsATPE) through the topical application, when through the spray method, with the highest percent mortality of 78.50% (dsATPD + dsCHS1). Our novel transdermal dsRNA delivery system not only provides a powerful tool for gene functional analysis in laboratory, but also shows a great potential for the pest management in the field, which will promote the practice and development of RNAi-based pest management.

Description of soybean aphid (Aphis glycines Matsumura) mitochondrial genome and comparative mitogenomics of Aphididae (Hemiptera: Sternorrhyncha)

The complete mitochondrial genome of the soybean aphid (Aphis glycines Matsumura), a major agricultural pest in the world, is described for the first time, which consists of 13 protein-coding genes, 22 tRNA genes, 2 rRNA genes, as well as a large repeat region between tRNA-Glu and tRNA-Phe, and an AT-rich control region. The 17,954 bp mtgenome is the largest reported from the family Aphididae, and its gene order follows the ancestral insect mtgenome except for the repeat region, which contains a 195 bp unit repeated 11.9 times, representing the highest reported repeats among the known aphid mtgenomes to date. A new molecular phylogeny of Aphidae is reconstructed based on all available aphid mtgenomes, and it is shown that the mtgenome data can robustly resolve relationships at the subfamily level, but do not have sufficient phylogenetic information to resolve deep relationships. A phylogeny-based comparative analysis of mtgenomes has been performed to investigate the evolution of the repeat region between tRNA-Glu and tRNA-Phe. So far, among aphids, 13 species are known to have this repeat region of variable lengths, and a phylogenetic analysis of the repeat region shows that a large proportion of the sequences are conserved across the phylogeny, suggesting that the repeat region evolved in the most recent common ancestor of Aphidinae and Eriosomatinae, and that it has gone through numerous episodes of lineage-specific losses and expansions. Combined together, this study provides novel insights into how the repeat regions have evolved within aphids.

BABA application improves soybean resistance to aphid through activation of phenylpropanoid metabolism and callose deposition.

Beta-aminobutyric acid (BABA) confer plant resistance to a broad spectrum of biotic and abiotic stresses. The soybean aphid (SBA), is native to eastern Asia and is a predominant insect pest of soybean. Both isoflavone and lignin pathway are important branches of the general phenylpropanoid pathway, which would be likely associated with resistance against soybean aphid. However, little is known about the role of the phenylpropanoid pathway in defense response to SBA as induced by BABA application. The application of BABA effectively enhanced soybean resistance against Aphis glycines, the soybean aphid. Consistent with significantly increased content of isoflavones, especially genistein, the related biosynthetic genes were upregulated by use of BABA. Lignin, another important defense component against arthropods, accumulated at a high level and four lignin biosynthesis related genes were also activated. Additionally, BABA application augmented the expression of callose synthase genes and increased callose deposition in SBA-infested seedlings. In non-caged and caged tests, SBA numbers were significantly reduced in BABA-treated seedlings. These results demonstrate that application of BABA has an obvious positive effect on soybean resistance to aphids, and this defense response partly depends on the potentiation of isoflavone biosynthesis and callose deposition. © 2019 Society of Chemical Industry.

Efficacy of afidopyropen against soybean aphid (Hemiptera: Aphididae) and toxicity to natural enemies.

Soybean aphid, Aphis glycines (Hemiptera: Aphididae), remains the most significant soybean insect pest in the North Central Region of the USA. The sustainability of reliance on only a few insecticide groups for this pest is questionable. We evaluate afidopyropen, a novel pyropene insecticide (Group 9D), for efficacy against A. glycines in field and greenhouse experiments and toxicity to common natural enemies in laboratory experiments. Across 4 site-years of field experiments and a greenhouse experiment, afidopyropen reduced A. glycines populations similar to commonly used broad-spectrum [i.e. lambda-cyhalothrin (Group 3A) and chlorpyrifos (Group 1B)] insecticides and potential selective insecticides [i.e. sulfoxaflor (Group 4C) and flupyradifurone (Group 4D)]. In the greenhouse, however, A. glycines mortality was delayed slightly for afidopyropen compared to the other insecticides. In laboratory experiments with natural enemies of A. glycines, afidopyropen was not toxic to adult or third instar Hippodamia convergens (Coleoptera: Coccinellidae) or adult Orius insidiosus (Hemiptera: Anthocoridae), and was only moderately toxic to Aphelinus certus (Hymenoptera: Aphelinidae). Afidopyropen is effective against A. glycines and relatively non-toxic to natural enemies, and appears to be an effective option for integrated pest management and insecticide resistance management programs for A. glycines. © 2019 Society of Chemical Industry.

Identification and expression profiles analysis of odorant‐binding proteins in soybean aphid, Aphis glycines (Hemiptera: Aphididae)

The soybean aphid, Aphis glycines, is an extreme specialist and an important invasive pest that relies on olfaction for behaviors such as feeding, mating, and foraging. Odorant-binding proteins (OBPs) play a vital role in olfaction by binding to volatile compounds and by regulating insect sensing of the environment. In this work we used rapid amplification of complementary DNA ends technology to identify and characterize 10 genes encoding A. glycines OBPs (AglyOBPs) belonging to 3 subfamilies, including 4 classic OBPs, 5 Plus-C OBPs, and one Minus-C OBP. Quantitative real-time polymerase chain reaction demonstrated variable specific expression patterns for the 10 genes based on developmental stage and aphid tissue sampled. Expression levels of 7 AglyOBPs (2, 3, 4, 5, 7, 9, and 10) were highest in the 4th instar, indicating that the 4th nymphal instar is an important developmental period during which soybean aphids regulate feeding and search for host plants. Tissue-specific expression results demonstrated that AglyOBP2, 7, and 9 exhibited significantly higher expression levels in antennae. Meanwhile, ligand-binding analysis of 5 OBPs demonstrated binding of AglyOBP2 and AglyOBP3 to a broad spectrum of volatiles released by green leaf plants, with bias toward 6- to 8-carbon chain volatiles and strong binding of AglyOBP7 to trans-β-farnesene. Taken together, our findings build a foundation of knowledge for use in the study of molecular olfaction mechanisms and provide insights to guide future soybean aphid research.

Transcriptome profiling of interaction effects of soybean cyst nematodes and soybean aphids on soybean

Soybean aphid (Aphis glycines; SBA) and soybean cyst nematode (Heterodera glycines; SCN) are two major pests of soybean (Glycine max) in the United States of America. This study aims to characterize three-way interactions among soybean, SBA, and SCN using both demographic and genetic datasets. SCN-resistant and SCN-susceptible soybean cultivars with a combination of soybean aphids (biotype 1) and SCN (HG type 0) in a randomized complete block design (RCBD) with six blocks were used to evaluate the three-way interactions in a greenhouse setup. Treatments receiving SCN were infested at planting with 2000 nematode eggs, and the treatments with soybean aphids were infested at second trifoliate growth stage (V2) with 15 soybean aphids. The whole roots were sampled from plants at 5 and 30 days post SBA infestation for RNA sequencing using Illumina Hiseq. 3000. The data comprises of 47 libraries that are useful for further analyses of important genes, which are involved in interaction effects of SBA and SCN on soybean.

Comparing performance of Aphis glycines Matsumura fed on two novel hosts relative to Glycine max (L.) Merrill

Abstract The soybean aphid, Aphis glycines Matsumura, is an important pest of soybean. During some years with occurrences of heavy aphid infestations in field, A. glycines can cause serious damage to soybeans. A. glycines has a heteroecious and holocyclic life cycle, with migration occurring between the primary and secondary hosts during each year. The primary hosts of A. glycines are Rhamnus spp., and the secondary hosts are soybean, Glycine max (L.) Merrill, and wild soybean species, Glycine soja Sieb & Zucc. In this study, A. glycines were fed on detached leaves and live plants of Trifolium repens L. and Metaplexis japonica (Thunb.) Makino, and their survival, development and reproduction were studied at five constant temperatures. These data were compared to those of controls fed on the known host plant G. max. When A. glycines were fed on detached leaves of T. repens and M. japonica, they showed vigorous development and reproduction. The novel and striking results were that: (1) A. glycines could not thrive on live plants of M. japonica, and only a few nymphs were deposited. (2) When A. glycines were fed on live plants of vegetative stage T. repens, adult longevity and fecundity were as long as 11.64 ± 1.17 days and as great as 12.92 ± 1.23 nymphs per adult, respectively. This work provides important evidence that M. japonica is not a host of A. glycines, but T. repens is probably an important host for this aphid.

Adjacent habitat type affects the movement of predators suppressing soybean aphids.

Landscape complexity influences soybean aphid suppression by generalist predators in North America, but the role of adjacent habitats as sources of these predators has not been studied directly. We quantified movement of aphidophagous predators between soybean and five adjacent habitats common in Manitoba using bi-directional Malaise traps. To test the contribution of predators from neighboring habitats to soybean aphid suppression, we performed experimental manipulations in adjacent soybean and alfalfa fields and monitored the movement of sevenspotted lady beetles, Coccinella septempunctata, using mark-release-recapture experiments. The identity of adjacent habitats affected the net movement of predators into soybean. The most abundant predators were hover flies (Diptera: Syrphidae), moving from woodlands to soybean. Similar (but non-significant) trends were found for lady beetles, minute pirate bugs, and green and brown lacewings. There was also a net movement of hover flies and green lacewings from soybean to canola. Lady beetles showed higher bidirectional movement in alfalfa and wheat borders than in woodland and canola borders in a high lady beetle abundance year. Soybean aphid populations in predator exclusion cages were 21- to 122- fold higher than populations exposed to predators, both in alfalfa and soybean fields. Aerial predators provide similar levels of aphid suppression as aerial and epigeal predators combined. Mark-release-recapture experiments showed high dispersal of C. septempunctata between soybean and alfalfa, with a net movement towards alfalfa, probably due to the lack of aphids in soybean. These results demonstrate that predator assemblages from both soybeans and alfalfa can suppress soybean aphids. Our findings indicate that the type of adjacent habitat and predator identity affect the directionality of predator movement into soybean. This study suggests that information on predator movement can be used to design the distribution of crops and natural habitats in agricultural landscapes that maximize pest control services.

A matrix model describing host-parasitoid population dynamics: The case of Aphelinus certus and soybean aphid.

Integrating elements from life tables into population models within a matrix framework has been an underutilized method of describing host–parasitoid population dynamics. This type of modeling is useful in describing demographically-structured populations and in identifying points in the host developmental timeline susceptible to parasitic attack. We apply this approach to investigate the effect of parasitism by the Asian parasitoid Aphelinus certus on its host, the soybean aphid (Aphis glycines). We present a matrix population model with coupled equations that are analogous to a Nicholson–Bailey model. To parameterize the model, we conducted several bioassays outlining host and parasitoid life history and supplemented these studies with data obtained from the literature. Analysis of the model suggests that, at a parasitism rate of 0.21 d−1, A. certus is capable of maintaining aphid densities below economically damaging levels in 31.0% of simulations. Several parameters—parasitoid lifespan, colonization timeline, host developmental stage, and mean daily temperature—were also shown to markedly influence the overall dynamics of the system. These results suggest that A. certus might provide a valuable service in agroecosystems by suppressing soybean aphid populations at relatively low levels of parasitism. Our results also support the use of A. certus within a dynamic action threshold framework in order to maximize the value of biological control in pest management programs.

Resistance of Soybean Plant Introductions to Three Colonies of Soybean Aphid (Hemiptera: Aphididae) Biotype 4.

Soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), infestations of soybean, Glycine max (L.) Merr. (Fabales: Fabaceae), and the associated yield loss have led to a large dependence on insecticidal management in soybean throughout the Midwestern United States. However, several populations of pyrethroid-resistant soybean aphids have recently been found in Iowa, Minnesota, North Dakota and South Dakota, which highlights the importance of alternative management approaches. One such alternative method is host-plant resistance, which uses naturally occurring plant defenses in crop cultivars to reduce the potential for yield loss from a pest population. Current soybean aphid-resistant cultivars do not protect against all soybean aphids due to the presence of virulent biotypes. In particular, soybean aphid biotype 4 is virulent to Rag1 and Rag2 resistance genes both individually and in combination. However, we hypothesized that resistance to biotype 4 may exist in previously identified, but uncharacterized resistant soybean plant introductions (PIs). To test this, we evaluated 51 previously identified but uncharacterized soybean aphid-resistant PIs for their resistance to colonies of soybean aphid biotype 4 collected in separate site-years (Lomira, WI 2013; Volga, SD 2015, 2016). Free-choice tests identified 14 PIs with putative resistance to 'Lomira13', two to 'Volga15', and eight to 'Volga16' soybean aphid colonies. Follow-up, no-choice tests corroborated two to three resistant PIs per colony, and PI 437696, which was resistant to each of the three colonies and could aid in breeding efforts and an integrated approach to soybean aphid management.

Resistance to soybean aphid biotype 4 in plant introductions of Glycine soja

Soybean aphid (Aphis glycines Matsumura) is a pest of soybean [Glycine max (L.) Merr] in the Midwestern U.S. and southern Canada. Host plant resistance provides an alternative to insecticides for soybean aphid management. Soybean with Rag1 + Rag2 aphid resistance is available commercially but does not protect against soybean aphid biotype 4 colonization. To find sources of resistance to soybean aphid biotype 4, we turned to soybean’s progenitor Glycine soja (Sieb. and Zucc.). Twenty soja plant introductions (PIs) with previously identified resistance to avirulent soybean aphid biotype 1 were assessed in free-choice tests against biotype 4, followed by a no-choice test for promising PIs. Experiments were repeated using three soybean aphid biotype 4 colonies, collected from separate site-years (Lomira, WI 2013; Volga, SD 2015, 2016). Free-choice tests identified six, three, and eight soja PIs with putative resistance to Lomira13, Volga15, and Volga16 aphid colonies, respectively. No-choice tests identified six, two, and six soja PIs that continued to suppress Lomira13, Volga15, and Volga16 aphids, respectively. PI 65549 and PI 101404A were resistant to each of the three colonies of soybean aphid biotype 4 and may contribute to durable resistance against soybean aphid.

Genetic mapping of soybean aphid biotype 3 and 4 resistance in PI 606390A

The soybean aphid (Aphis glycines Matsumura) is a pest of soybean (Glycine max (L.) Merr.) in many soybean-growing countries of the world, mainly in Asia and North America. While numerous aphid-resistance loci have been mapped, new and virulent aphid biotypes continue to be identified. PI 606390A confers resistance to all four characterized soybean aphid biotypes. The objectives of this study were to identify single nucleotide polymorphism (SNP) markers closely linked to the loci conferring resistance to soybean aphid biotypes 3 and 4. One hundred and eight F6:7 families from a cross between the susceptible experimental line HR09-018 and the resistant PI 606390A plus the two parental lines were screened with aphid biotypes 3 and 4 using greenhouse choice tests. Broad-sense heritability estimates ranged from 0.69 to 0.91. Correlation between biotype 3 and biotype 4 resistance was also moderate (45–55%). A total of 1847 SNP markers were mapped to 22 linkage groups, and loci for resistance to both aphid biotypes were mapped to a 14 cM region on chromosome 18 using composite interval mapping. The locus explained between 26 and 40% of the phenotypic variation suggests the presence of a major locus and additional unidentified minor quantitative trait loci (QTL). A new symbol qRag-G is proposed to designate this new locus that will be useful for the development of durable aphid-resistant soybean cultivars.

Transcriptional and Chemical Changes in Soybean Leaves in Response to Long-Term Aphid Colonization.

Soybean aphids (Aphis glycines Matsumura) are specialized insects that feed on soybean (Glycine max) phloem sap. Transcriptome analyses have shown that resistant soybean plants mount a fast response that limits aphid feeding and population growth. Conversely, defense responses in susceptible plants are slower and it is hypothesized that aphids block effective defenses in the compatible interaction. Unlike other pests, aphids can colonize plants for long periods of time; yet the effect on the plant transcriptome after long-term aphid feeding has not been analyzed for any plant–aphid interaction. We analyzed the susceptible and resistant (Rag1) transcriptome response to aphid feeding in soybean plants colonized by aphids (biotype 1) for 21 days. We found a reduced resistant response and a low level of aphid growth on Rag1 plants, while susceptible plants showed a strong response consistent with pattern-triggered immunity. GO-term analyses identified chitin regulation as one of the most overrepresented classes of genes, suggesting that chitin could be one of the hemipteran-associated molecular pattern that triggers this defense response. Transcriptome analyses also indicated the phenylpropanoid pathway, specifically isoflavonoid biosynthesis, was induced in susceptible plants in response to long-term aphid feeding. Metabolite analyses corroborated this finding. Aphid-treated susceptible plants accumulated daidzein, formononetin, and genistein, although glyceollins were present at low levels in these plants. Choice experiments indicated that daidzein may have a deterrent effect on aphid feeding. Mass spectrometry imaging showed these isoflavones accumulate likely in the mesophyll cells or epidermis and are absent from the vasculature, suggesting that isoflavones are part of a non-phloem defense response that can reduce aphid feeding. While it is likely that aphid can initially block defense responses in compatible interactions, it appears that susceptible soybean plants can eventually mount an effective defense in response to long-term soybean aphid colonization.