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Current Research on Soybean Aphid

Research Overview: In 2000, the soybean aphid, Aphis glycines, native to Asia, was found colonizing soybean plants in the Midwest USA. The pest has since spread throughout all soybean production areas in North America and has become established as the most important pest threatening soybean production. It can reduce yields directly when large populations colonize plants and divert photosythates away from seed production, and indirectly by spreading virus diseases such as Soybean mosaic virus. Large outbreaks of the soybean aphid have occurred in the Midwest and in Canada, especially in 2003, requiring producers to spend millions of dollars applying registered insecticides to minimize yield losses.

Publications

Chirumamilla, A., Hill, C.B., and Hartman, G.L. 2014. Stability of soybean aphid resistance in soybean across different temperatures. Crop Science 54: 2557-2563. doi:10.2135/cropsci2014.05.0393. [view abstract]
The soybean aphid (Aphis glycines Matsumura) is the most important insect pest posing a threat to soybean [Glycine max (L.) Merr.] grain production in the United States. Soybean cultivars with resistance are currently being deployed to aid in management of the pest. Temperature has been reported to influence the expression of host plant resistance against crop pests. The objective of this study was to determine if temperatures, 14, 21, and 28°C, altered resistance expression in four aphid-resistant soybean genotypes, LD05-16611 (with the Rag1 resistance gene), PI 200538 (Rag2), PI 567541B (rag1c, rag4), and PI 567597C (antixenosis) compared to a susceptible soybean genotype (Williams 82) when challenged with soybean aphid. A replicated no-choice experiment was conducted and aphid populations of the three soybean aphid biotypes, 1, 2, and 3, were enumerated 14 d after inoculating the five soybean genotypes. Significant interactions were found in the analysis of the effects of temperature, soybean genotype, and aphid biotype on aphid populations. Responses between soybean genotypes and aphid biotypes were consistent with previous reports with the exception of PI 567541B, which had lower resistance against aphid biotype 1 than found in an earlier study. At 14°C, there was limited aphid population growth on all soybean genotypes, including Williams 82. At 21 and 28°C, resistance expression was stable in LD05-16611 (Rag1), PI 567541B (rag1c, rag4), and PI 567597C (antixenosis), relative to susceptible Williams 82; however, resistance expressed in PI 200538 (Rag2) was significantly stronger at 28°C than at 21°C, as indicated by differences in aphid population size that were found. Results of this study indicated that soybean aphid virulence variability had a stronger influence on the effectiveness of soybean aphid resistance than did temperature, and that the aphid resistance tested in this study would remain stable or be stronger in temperatures ranging between 21 and 28°C.
Richardson M., Lagos D., Mitchell R., Hartman G.L., and Voegtlin D.J. 2011. Life history and morphological plasticity of the soybean aphid, Aphis glycines. Entomologia Experimentalis et Applicata 140:139–145. DOI: 10.1111/j.1570-7458.2011.01144.x.

Biology and Ecology

Hill, C.B., K.S. Kim, L. Crull, B.W. Diers, and G.L. Hartman. 2009. Inheritance of resistance to the soybean aphid in soybean PI200538. Crop Science 49: 1193-1200. [download] [view abstract]
The soybean aphid (Aphis glycines Matsumura) is a major soybean [Glycine max (L.) Merr.] insect pest. Soybean plant introduction (PI) 200538 has strong resistance to the aphid. The objectives of our research were to determine the inheritance of resistance and to map gene(s) controlling resistance in PI 200538. F2 populations developed from crosses between PI 200538 and three susceptible genotypes were tested for resistance and with DNA markers. F2 plants from the cross ‘Ina’ × PI 200538 segregated 114 resistant to 37 susceptible and F2 plants from the cross ‘Williams 82’ × PI 200538 segregated 203 resistant to 65 susceptible when tested for resistance to soybean aphid biotype 1. F2 plants from the cross LD02-4485 × PI 200538 segregated 167 resistant to 62 susceptible when tested for resistance to biotype 2. These populations fit a 3:1 genetic ratio (P = 0.89, 0.78, and 0.52, respectively) with resistance dominant over susceptibility. Segregation among F2:3 families from the crosses supported the dominant resistance gene hypothesis. The gene mapped to soybean linkage group F, flanked by the simple sequence repeat marker loci Satt510, Soyhsp176, Satt114, and Sct_033, located in the same region as the aphid resistance gene Rag2. Since the resistance gene in PI 200538 also gave resistance to soybean aphid biotypes 1 and 2, it is possible that the gene is Rag2 and not a new aphid resistance gene. Therefore, PI 200538 may be an additional source of Rag2.

Host-Pathogen Interaction

Domier, L. L., Latorre, I. J., Steinlage, T. A., McCoppin, N., and Hartman, G. L. 2003. Variability and transmission of Aphis glycines of North American and Asian soybean mosaic virus isolates. Archives of Virology 148:1925-1941. [link]
Domier, L. L., Steinlage, T. A., Hobbs, H. A., Yang, Y., Herrera-Rodriguez, G., Haudenshield, J. S., McCoppin, N. K., and Hartman, G. L. 2007. Similarities in seed and aphid transmission among Soybean mosaic virus isolates. Plant Disease 91: 546-550. [download] [view abstract]
Soybean mosaic virus (SMV) is an aphid- and seed-transmitted virus that infects soybean (Glycine max) plants and causes significant yield losses. Seed-borne infections are the primary sources of inoculum for SMV infections. The strain specificity of SMV transmission through seed and SMV-induced seed-coat mottling were investigated in field experiments. Six soybean plant introductions (PIs) were inoculated with eight SMV strains and isolates. Transmission of SMV through seed ranged from 0 to 43%, and isolate-by-soybean line interactions occurred in both transmission rates and percentages of mottled seeds. For example, SMV 746 was transmitted through 43% of seed in PI 229324, but was not transmitted through seed of PIs 68522, 68671, or 86449. In contrast, SMV 413 was transmitted through seed from all PIs. SMVs that were transmitted poorly by the Asian soybean aphid, Aphis glycines, also were transmitted poorly through seed. No predicted amino acid sequences within the helper-component protease or coat protein coding regions differentiated the two groups of SMV strains. The loss of aphid and seed transmissibility by repeated mechanical transmission suggests that constant selection pressure is needed to maintain the regions of the SMV genome controlling the two phenotypes from genetic drift and loss of function.
Hill, C.B., Chirumamilla, A. and Hartman, G.L. 2012. Resistance and virulence in the soybean-Aphis glycines interaction. Euphytica 186:635–646. [view abstract]
Aphis glycines Matsumura, the soybean aphid, first arrived in North America in 2000 and has since become the most important insect pest of domestic soybean, causing significant yield loss and increasing production costs annually in many parts of the USA soybean belt. Research to identify sources of resistance to the pest began shortly after it was found and several sources were quickly identified in the USDA soybean germplasm collection. Characterization of resistance expression and mapping of resistance genes in resistant germplasm accessions resulted in the identification of six named soybean aphid resistance genes: Rag1, rag1c, Rag2, Rag3, rag4, and Rag5 (proposed). Simple sequence repeat markers flanking the resistance genes were identified, facilitating efforts to use marker-assisted selection to develop resistant commercial cultivars. Saturation or fine-mapping with single nucleotide polymorphism markers narrowed the genomic regions containing Rag1 and Rag2 genes. Two potential NBS-LRR candidate genes for Rag1 and one NBS-LRR gene for Rag2 were found within the regions. Years before the release of the first resistant soybean cultivar with Rag1 in 2009, a soybean aphid biotype, named biotype 2, was found that could overcome the resistance gene. Later in 2010, biotype 3 was characterized for its ability to colonize plants with Rag2 and other resistance genes. At present, three biotypes have been reported that can be distinguished by their virulence on Rag1 and Rag2 resistance genes. Frequency and geographic distribution of soybean aphid biotypes are unknown. Research is in progress to determine the inheritance of virulence and develop DNA markers tagging virulence genes to facilitate monitoring of biotypes. With these research findings and the availability of host lines with different resistance genes and biotypes, the soybean aphid-soybean pest-host system has become an important model system for advanced research into the interaction of an aphid with its plant host, and also the tritrophic interaction that includes aphid endosymbionts.
Hill, C.B., Crull, L., Herman, T.K., Voegtlin, D.J. and Hartman, G.L. 2010. A new soybean aphid (Hemiptera: Aphididae) biotype identified. J. Economic Entomology 103:509-515. [link]
Hill, C. B., Li, Y., and Hartman, G. L. 2004. Resistance of Glycine species and various cultivated legumes to the soybean aphid (Homoptera: Aphididae). J. of Econ. Entomol. 97:1071-1077. [download] [view abstract]
ABSTRACT The soybean aphid, Aphis glycines Matsumura, is a new pest of soybean, Glycine max (L.) Merr., in North America. It has become widespread on soybean in North America since it was first identifed in the Midwest in 2000. Species of Rhamnus L. (buckthorn) are the primary hosts of A. glycines, and soybean is known as a secondary host. There is limited information about the secondary host range of A. glycines. Aphid colonization on variouslegume hostswascompared in choice experiments. Aphid colonization occurred on species in the genus Glycine Wild. No colonization occurred on Lablab purpureus (L.) Sweet, Lens culinaris Medik, Phaseolus vulgaris L., Pisum sativum L., or species of Vicia L. and Vigna Savi. Colonization was limited or aphids were transient on species of Medicago L., Phaseolus L., and Trifolium L. There were significant differences in aphid colonization among Medicago truncatula accessions with numbers ranging from 7 to 97 aphids per plant. Six Glycine soja Sieb.&Zucc. accessions were as resistant as G. max accessions to A. glycines; these may represent novel sources of A. glycines resistance not found in G. max. Antibiosis was found to play a large role in the expression of resistance in three of the G. soja accessions. Results of this study indicated that G. max and G. soja were the best secondary hosts of A. glycines; however, its secondary host range may include other leguminous species. Therefore, A. glycines did not seem to have a highly restricted monophagous secondary host range.
Hill, C. B., Li, Y., and Hartman, G. L. 2004. Resistance to the soybean aphid in soybean germplasm. Crop Sci. 44:98-106. [download] [view abstract]
With an efficient greenhouse screening method, the first resistance to the soybean aphid (Aphis glycines Matsumura) was found in culti¬vated soybean [Glycine max (L.) Merr.] germplasm. No resistance was found in 1425 current North American soybean cultivars, 106 Maturity Group (MG) 000 through VII Asian cultivars, and in a set of 11 'Clark' isolines possessing different pubescence traits. Dense pubescence did not provide protection against the soybean aphid. Resistance was discovered and established in three ancestors of North American genotypes: 'Dowling', 'Jackson', and PI 71506. Expression of resis¬tance in those genotypes was characterized in choice and nonchoice tests. In choice tests, significantly fewer aphids occurred on Dowling, Jackson, and PI 71506 plants compared with susceptible cultivars (P = 0.05). Aphid populations did not develop on Dowling and Jackson in nonchoice tests, indicating that there was a negative impact on aphid fecundity on those cultivars. That evidence combined with ob¬servations of aphid mortality on those cultivars suggested that antibio¬sis-type resistance contributed to the expression of resistance. Possible donors of resistance to Dowling and Jackson were identified. In non-choice tests, population development on PI 71506 was not sig¬nificantly different from development on susceptible cultivars, indicat¬ing that antixenosis was more important in that genotype. Resistance was expressed in all plant stages. Dowling provided season-long pro¬tection against aphids equal to the use of the systemic insecticide imi-dadoprid {l-[(6-Chloro-3-pyridinyl)methyl]-Ar-nitro-2-imidazolidini-mine) in a field test. Four other germplasm accessions, 'Sugao Zarai', 'Sato', 'T260H', and PI 230977, had levels of resistance not significantly different from Dowling, Jackson, and PI 71506 in a choice test (P = 0.05).
Hill, C. B., Li, Y., and Hartman, G. L. 2006. A single dominant gene for resistance to the soybean aphid in the soybean cultivar Dowling. Crop Science 46:1601-1605. [download] [view abstract]
The soybean aphid (Aphis glycines Matsumura), a new pest of soybean [Glycine max (L.) Merr.], rapidly spread throughout North America after its arrival in 2000 and caused millions of dollars in economic losses. At present, the application of insecticides is the only means to control the soybean aphid. However, genetic resistance to the aphid was recently discovered in soybean germplasm and the soybean cultivar Dowling was identified as having strong antibiosis-type aphid resistance. The objective of this study was to determine the inheritance of resistance to the soybean aphid in Dowling. Resistance in F1, F2, and F2–derived F3 (F2:3) families from crosses between Dowling and the two susceptible soybean cultivars Loda and Williams 82 was analyzed. All F1 plants were resistant to the aphid. Heterogeneity of segregation of F2 plants in 14 Dowling x Loda F2 families was nonsignificant (P = 0.16), and pooled F2 data, with 132 resistant to 45 susceptible plants, fit a 3:1 ratio (P = 0.90). F2 plants from Dowling x Williams 82 segregated 135 resistant to 44 susceptible, also fitting a 3:1 ratio (P = 0.89). Segregation among the F2:3 families fit a 1:2:1 monogenic inheritance pattern. These results indicated that a single dominant gene named Rag1 controlled resistance in Dowling. The monogenic dominant nature of resistance will enable breeders to rapidly convert existing susceptible cultivars to resistant cultivars using backcrossing procedures.
Hill, C. B., Li, Y., and Hartman, G. L. 2006. Soybean aphid resistance in soybean Jackson is controlled by a single dominant gene. Crop Science 46:1606-1608. [download] [view abstract]
The soybean aphid, Aphis glycines Matsumura, has become established as a serious pest of soybean, Glycine max (L.) Merr., since it was first found in North America in 2000 and has caused millions of dollars in economic losses. While the application of chemical insecticides is the only means to control the soybean aphid at present, genetic resistance to the aphid was recently discovered in soybean. A single dominant gene named Rag1 that controls resistance to the soybean aphid was found in the cultivar Dowling. Another cultivar found to have strong antibiosis-type resistance to the soybean aphid was Jackson. The primary objective of this study was to determine the inheritance of resistance to the soybean aphid in Jackson. Segregation of resistance was analyzed in F2 and among F2–derived F3 (F2:3) families produced from crosses between Jackson and the susceptible soybean cultivar Loda. Segregation of F2 plants was 247 resistant to 97 susceptible and fit a 3:1 genetic ratio (P = 0.17). Segregation among F2:3 families was not clear because a number of susceptible F2 plants did not produce a sufficient amount of seed for progeny testing. Ignoring the susceptible class, the segregation of F2:3 families fit a 1:2 (all resistant/segregating) ratio. These results indicated that a single dominant gene controlled resistance in Jackson. There is no known genetic relationship between Jackson and Dowling. The genetic relationship between Rag1 in Dowling and the gene in Jackson is unknown.
Kim, K.-S., C.B. Hill, G.L. Hartman, D. Hyten, M.E. Hudson, and B.W. Diers. 2010. Fine mapping of the soybean aphid resistance gene Rag2 in soybean PI 200538. Theoretical Applied Genetics 121: 599-610. [link]
Kim, K. S., Hill, C. B., Hartman, G. L., Mian, M. A. R., and Diers, B. W.2008. Discovery of soybean aphid biotypes. Crop Science 48:923-928. [download] [view abstract]
The soybean aphid [Aphis glycines Matsumura (Hemiptera: Aphididae)] is an invasive insect pest of soybean [Glycine max (L.) Merr.] that was first reported in North America in 2000. There are currently no reports of soybean aphid biotype diversity and this information is needed before aphid resistance genes are deployed. The objective of this research was to test for aphid biotype variation. The response of two A. glycines isolates, one collected in Ohio and the other in Illinois, were compared by infesting eight soybean genotypes in nonchoice tests. The same genotypes also were tested with the Ohio isolate using a choice test. In the nonchoice test, there was a significant (P < 0.0001) effect of aphid isolate, genotype, and a significant aphid isolate by soybean genotype interaction for the number of aphids per plant 10 and 15 d after infestation. The responses of the eight genotypes to the Ohio isolate in the choice test were similar to their responses in nonchoice tests. PI 200538 and PI 567597C were resistant to both the Ohio and Illinois isolates and will be useful sources of resistance to both isolates. These tests confirm that there are at least two distinct biotypes of A. glycines in North America.
Kim, K.S., S. Bellendir, K.A. Hudson, C.B. Hill, G.L. Hartman, D.L. Hyten, M.E. Hudson and B.W. Diers. 2010. Fine mapping the soybean aphid resistance gene Rag1 in soybean. Theoretical & Applied Genetics 120:1063-1071. [link]
Li, Y., Hill, C. B., and Hartman, G. L. 2004. Effect of three resistant soybean genotypes on the fecundity, mortality, and maturation of the soybean aphid, Aphis glycines (Homoptera: Aphididae). Journal of Economic Entomology 97:1106-1111. [download] [view abstract]
The fecundity, longevity, mortality, and maturation of the soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae), were characterized using three resistant soybean, Glycine max (L.) Merrill, genotypes ('Dowling', 'Jackson', and PI200538 'Sugao Zarai') and two susceptible genotypes ('Pana' and 'Loda'). Antibiosis in the resistant genotypes was demonstrated by a significant decrease in fecundity and longevity and increased mortality of A. glycines. Aphid fecundity, measured as number of offspring produced in the first 10 d by each viviparous aptera, was higher on Pana than on the resistant genotypes. Aphid longevity, the mean number of days a 1-d-old adult lived, was 7 d longer on Pana than on Dowling and Jackson. The mortality of both viviparous apterae and nymphs on resistant genotypes was significantly higher than on susceptible genotypes. A greater number of first instars survived to maturation stage (date of first reproduction) on susceptible plants than on resistant plants. None of the first instars placed on Dowling and PI200538 leaves survived to maturation. Observations of aphid behavior on leaves indicated that aphids departed from the leaves of resistant plants 8 -24 h after being placed on them, whereas they remained indefinitely on leaves of susceptible cultivars and developed colonies. Reduced feeding due to ingestion of potentially toxic compounds in soybean may explain the possible mechanism of resistance to the soybean aphid. KEY WORDS Aphis glycines, aphid longevity, feeding preferences, host resistance, soybean aphid.
Li, Y., Hill, C. B., Carlson, S. R., Diers, B. W., and Hartman, G. L. 2007. Soybean aphid resistance genes in the soybean cultivars Dowling and Jackson map to linkage group M. Molecular Breeding 19: 25-34. [link]
Li, Y., Zou, J., Li, M., Bilgin, D. D., Vodkin, L. O., Hartman, G. L., and Clough, S. J. 2008. Soybean defense responses to the soybean aphid. New Phytologist 179: 185–195. [download] [view abstract]
Transcript profiles in aphid (Aphis glycines)-resistant (cv. Dowling) and -susceptible (cv. Williams 82) soybean (Glycine max) cultivars using soybean cDNA microarrays were investigated. Large-scale soybean cDNA microarrays representing approx. 18 000 genes or c. 30% of the soybean genome were compared at 6 and 12 h post-application of aphids. In a separate experiment utilizing clip cages, expression of three defense-related genes were examined at 6, 12, 24, 48, and 72 h in both cultivars by quantitative real-time PCR. One hundred and forty genes showed specific responses for resistance; these included genes related to cell wall, defense, DNA/RNA, secondary metabolism, signaling and other processes. When an extended time period of sampling was investigated, earlier and greater induction of three defense-related genes was observed in the resistant cultivar; however, the induction declined after 24 or 48 h in the resistant cultivar but continued to increase in the susceptible cultivar after 24 h. Aphid-challenged resistant plants showed rapid differential gene expression patterns similar to the incompatible response induced by avirulent Pseudomonas syringae. Five genes were identified as differentially expressed between the two genotypes in the absence of aphids.

Epidemiology and Management

Hartman, G. L., Domier, L. L., Wax, L. M., Helm, C. G., Onstad, D. W., Shaw, J. T., Solter, L. F., Voegtlin, D. J., D'Arcy, C. J., Gray, M. E., Steffey, K. L., Isard, S. A., and Orwick, P. L. 2001. Occurrence and distribution of Aphis glycines on soybeans in Illinois in 2000 and its potential control. Plant Health Progess:(On-line). [download]
<em>Aphis glycines</em> Matsumura, soybean aphid. Aphis glycines Matsumura, soybean aphid.
Soybean cultivar susceptible  to soybean aphid (left), and one showing resistance (right). Soybean cultivar susceptible to soybean aphid (left), and one showing resistance (right).
Soybean aphids massing on a soybean stem. Soybean aphids massing on a soybean stem.