Michael T. McCarville

One gene versus two: A regional study on the efficacy of single gene versus pyramided resistance for soybean aphid management

ABSTRACT The soybean aphid (Aphis glycines Matsumura) is a threat to soybean production in the Midwestern United States. Varieties containing the Rag1 soybean aphid resistance gene have been released with limited success in reducing aphid populations. Furthermore, virulent biotypes occur within North America and challenge the durability of single-gene resistance. Pyramiding resistance genes has the potential to improve aphid population suppression and increase resistance gene durability. Our goal was to determine if a pyramid could provide improved aphid population suppression across a wide range of environments.Weconducted a small-plot field experiment across seven states and three years. We compared soybean near-isolines for the Rag1 or Rag2 gene, and a pyramid line containing both genes for their ability to decrease aphid pressure and protect yield compared with a susceptible line. These lines were evaluated both with and without a neonicitinoid seed treatment. All aphid-resistant lines significantly decreased aphid pressure at all locations but one. The pyramid line experienced lower aphid pressure than both single-gene lines at eight of 23 location-years. Soybean aphids significantly reduced soybean yield for the susceptible line by 14% and for both single-gene lines by 5%; however, no significant yield decrease was observed for the pyramid line. The neonicitinoid seed treatment reduced plant exposure to aphids across all soybean lines, but did not provide significant yield protection for any of the lines. These results demonstrate that pyramiding resistance genes can provide sufficient and consistent yield protection from soybean aphid in North America.

Measuring the Benefit of Biological Control for Single Gene and Pyramided Host Plant Resistance for Aphis glycines (Hemiptera: Aphididae) Management

ABSTRACT The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is an economically important pest in the north central United States. In the state of Iowa, economically damaging populations occurred in seven of 11 growing seasons from 2001 to 2011. The high frequency and economic impact of the soybean aphid makes it an ideal candidate for management by using host plant resistance. We compared an aphid-susceptible line to near-isolines that contain Rag1 and Rag2, both alone and pyramided together, to suppress aphid populations and protect yield. Each of four near-isolines, were artificially infested with aphids and grown in small plots in which the exposure to natural enemies was controlled by the use of cages, resulting in the following treatment groups: natural enemy free (only aphids),biocontrol (both aphids and natural enemies), and aphid free (no aphids or natural enemies). The seasonal accumulation of aphids and the population growth rates were measured for each line and an estimate of yield was measured at the end of the season. Soybean aphid population growth rate was reduced 20% by natural enemies alone, 44% by pyramided resistance, and 63% by the combination of natural enemies and pyramided resistance. This reduction in population growth rate resulted in a 99.3% reduction in the pyramid lines seasonal exposure to aphids. In the presence of natural enemies, all three resistant lines maintained aphid populations below the economic injury level and prevented yield loss. This study demonstrates the compatibility of biological control with soybean aphid host plant resistance and its utility, especially for single resistance gene lines.

A nematode, fungus, and aphid interact via a shared host plant: implications for soybean management

Soybean, Glycine max (L.) Merrill (Fabaceae), is an introduced crop to America and initially benefited from a small number of pests threatening its production. Since its rapid expansion in production beginning in the 1930s, several pests have been introduced from the native range of soybean. Our knowledge of how these pests interact and the implications for management is limited. We examined how three common economic soybean pests, the nematode Heterodera glycines Ichinohe (Nematoda: Heteroderidae), the fungus Cadophora gregata Harrington & McNew (Incertae sedis), and the aphid Aphis glycines Matsumura (Hemiptera: Aphididae), interact on soybean cyst nematode‐susceptible (SCN‐S) and soybean cyst nematode‐resistant cultivars carrying the PI 88788 resistance source (SCN‐R). From 2008 to 2010, six soybean cultivars were infested with either a single pest or all three pests in combination in a micro‐plot field experiment. Pest performance was measured in a ‘single pest’ treatment and compared with pest performance in the ‘multiple pest’ treatment, allowing us to measure the impact of SCN resistance and the presence of other soybean pests on each pest’s performance. Performance of H. glycines (80% reduction in reproduction) and A. glycines (19.8% reduction in plant exposure) was reduced on SCN‐R cultivars. Regardless of cultivar, the presence of multiple pests significantly decreased the performance of A. glycines, but significantly increased H. glycines performance. The presence of multiple pests decreased the performance of C. gregata on SCN‐S soybean cultivars (20.6% reduction in disease rating).

An Induced Susceptibility Response in Soybean Promotes Avirulent Aphis glycines (Hemiptera: Aphididae) Populations on Resistant Soybean

ABSTRACT Observations of virulent Aphis glycines Matsumura populations on resistant soybean in North America occurred prior to the commercial release of Rag genes. Laboratory assays confirmed the presence of four A. glycines biotypes in North America defined by their virulence to the Rag1 and Rag2 genes. Avirulent and virulent biotypes can co-occur and potentially interact on soybean, which may result in induced susceptibility. We conducted a series of experiments to determine if the survival of avirulent biotypes on susceptible and resistant soybean containing the Rag1 or Rag1 + Rag2 genes was affected by the presence of either avirulent or virulent conspecifics. Regardless of virulence to Rag genes, initial feeding by conspecifics increased the survival of subsequent A. glycines populations on both susceptible and resistant soybean. Avirulent populations increased at the same rate as virulent populations if the resistant plants were initially colonized with virulent aphids. These results are the first to demonstrate that virulent A. glycines increase the suitability of resistant soybean for avirulent conspecifics, thus explaining the lack of genetic differentiation observed in North America between A. glycines populations on resistant and susceptible soybean. These results suggest the occurrence of virulence toward Rag genes in North America may be overestimated. In addition this may alter the selection pressure for virulence genes to increase in a population. Therefore, insect resistance management models for A. glycines may need to incorporate induced susceptibility factors to determine the relative durability of resistance genes.

Soybean Aphid (Aphididae: Hemiptera) Population Growth as Affected by Host Plant Resistance and an Insecticidal Seed Treatment

ABSTRACT The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) is a significant soybean pest in the north central United States. Insecticidal seed treatments and host plant resistance are two commercially available management tools. Here we investigate the efficacy of both management tools throughout the season. Soybean lines containing the soybean aphid resistance genes Rag1, Rag2, or both Rag1 + Rag2 were compared with a near-isogenic aphid-susceptible line. Each line was grown in field plots both with and without thiamethoxam applied to the seed. Individual plants from each plot were caged and infested with soybean aphids to measure the efficacy and potential interaction of aphid resistance and thiamethoxam. Aphid population growth rate was measured for each caged plant for 9–12 d after infestation. New cages were established each week from 34 d after planting (dap) to 92 dap to track seasonal variations in efficacy. Thiamethoxam reduced population growth only at the 42 dap time point and only for the susceptible, Rag1, and Rag2 lines. The lack of an effect of thiamethoxam on the Rag1 + Rag2 line was likely because of already high mortality from two resistance genes. Aphid resistance alone reduced population growth compared with the susceptible line at least till 55 dap for single-gene resistance and 63 dap for the two genes combined. Aphid resistance provided suppression of soybean aphid population growth throughout the season unlike the insecticidal seed treatment.

Reduced Fitness of Virulent Aphis glycines (Hemiptera: Aphididae) Biotypes May Influence the Longevity of Resistance Genes in Soybean

Sustainable use of insect resistance in crops require insect resistance management plans that may include a refuge to limit the spread of virulence to this resistance. However, without a loss of fitness associated with virulence, a refuge may not prevent virulence from becoming fixed within a population of parthenogenetically reproducing insects like aphids. Aphid-resistance in soybeans (i.e., Rag genes) prevent outbreaks of soybean aphid (Aphis glycines), yet four biotypes defined by their capacity to survive on aphid-resistant soybeans (e.g., biotype-2 survives on Rag1 soybean) are found in North America. Although fitness costs are reported for biotype-3 on aphid susceptible and Rag1 soybean, it is not clear if virulence to aphid resistance in general is associated with a decrease in fitness on aphid susceptible soybeans. In laboratory assays, we measured fitness costs for biotype 2, 3 and 4 on an aphid-susceptible soybean cultivar. In addition, we also observed negative cross-resistance for biotype-2 on Rag3, and biotype-3 on Rag1 soybean. We utilized a simple deterministic, single-locus, four compartment genetic model to account for the impact of these findings on the frequency of virulence alleles. When a refuge of aphid susceptible was included within this model, fitness costs and negative cross-resistance delayed the increase of virulence alleles when virulence was inherited recessively or additively. If virulence were inherited additively, fitness costs decreased the frequency of virulence. Combined, these results suggest that a refuge may prevent virulent A. glycines biotypes from overcoming Rag genes if this aphid-resistance were used commercially in North America.

Aboveground Feeding by Soybean Aphid, Aphis glycines, Affects Soybean Cyst Nematode, Heterodera glycines, Reproduction Belowground

Heterodera glycines is a cyst nematode that causes significant lost soybean yield in the U.S. Recent studies observed the aphid Aphis glycines and H. glycines interacting via their shared host, soybean, Glycine max. A greenhouse experiment was conducted to discern the effect of A. glycines feeding on H. glycines reproduction. An H. glycines-susceptible cultivar, Kenwood 94, and a resistant cultivar, Dekalb 27–52, were grown in H. glycines-infested soil for 30 and 60 d. Ten days after planting, plants were infested with either zero, five, or ten aphids. At 30 and 60 d, the number of H. glycines females and cysts (dead females) and the number of eggs within were counted. In general, H. glycines were less abundant on the resistant than the susceptible cultivar, and H. glycines abundance increased from 30 to 60 d. At 30 d, 33% more H. glycines females and eggs were produced on the resistant cultivar in the ten-aphid treatment compared to the zero-aphid treatment. However, at 30 d the susceptible cultivar had 50% fewer H. glycines females and eggs when infested with ten aphids. At 60 d, numbers of H. glycines females and cysts and numbers of eggs on the resistant cultivar were unaffected by A. glycines feeding, while numbers of both were decreased by A. glycines on the susceptible cultivar. These results indicate that A. glycines feeding improves the quality of soybean as a host for H. glycines, but at higher herbivore population densities, this effect is offset by a decrease in resource quantity.

What is the Economic Threshold of Soybean Aphids (Hemiptera: Aphididae) in Enemy-Free Space?

ABSTRACT Soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is a serious pest of soybean, Glycine max (L.) Merr., in the North Central United States. Current management recommendations rely on the application of insecticides based on an economic threshold (ET) of 250 aphids per plant. Natural enemies are important in slowing the increase of aphid populations and can prevent them from reaching levels that can cause economic losses. However, biological control of A. glycines is inconsistent and can be affected negatively by the intensity of agricultural activity. We measured the impact of a natural-enemy-free environment on the capacity of the current ET to limit yield loss. In 2008 and 2009, caged microplots were assigned to one of three treatments: plants kept aphid-free (referred to as the control), plants that experienced a population of 250 aphids per plant (integrated pest management [IPM]), and plants that experienced unlimited aphid population growth (unlimited). The population growth rate of aphids in the unlimited treatment for the 10 d after the application of insecticides to the IPM treatment was calculated using linear regression. The linear equation was solved to determine the mean number of days between the ET and the EIL for an aphid population in absence of predators. The number of days was determined to be 6.97 ± 1.11 d. The 2-yr average yield for the IPM treatment was 99.93% of the control treatment. Our study suggests the current soybean aphid ET of 250 aphids per plant can effectively protect yield even if the impact of natural enemies is reduced.

Soybean Aphid Infestation Induces Changes in Fatty Acid Metabolism in Soybean

The soybean aphid (Aphis glycines Matsumura) is one of the most important insect pests of soybeans in the North-central region of the US. It has been hypothesized that aphids avoid effective defenses by inhibition of jasmonate-regulated plant responses. Given the role fatty acids play in jasmonate-induced plant defenses, we analyzed the fatty acid profile of soybean leaves and seeds from aphid-infested plants. Aphid infestation reduced levels of polyunsaturated fatty acids in leaves with a concomitant increase in palmitic acid. In seeds, a reduction in polyunsaturated fatty acids was associated with an increase in stearic acid and oleic acid. Soybean plants challenged with the brown stem rot fungus or with soybean cyst nematodes did not present changes in fatty acid levels in leaves or seeds, indicating that the changes induced by aphids are not a general response to pests. One of the polyunsaturated fatty acids, linolenic acid, is the precursor of jasmonate; thus, these changes in fatty acid metabolism may be examples of “metabolic hijacking” by the aphid to avoid the induction of effective defenses. Based on the changes in fatty acid levels observed in seeds and leaves, we hypothesize that aphids potentially induce interference in the fatty acid desaturation pathway, likely reducing FAD2 and FAD6 activity that leads to a reduction in polyunsaturated fatty acids. Our data support the idea that aphids block jasmonate-dependent defenses by reduction of the hormone precursor.

Increase in Soybean Cyst Nematode Virulence and Reproduction on Resistant Soybean Varieties in Iowa From 2001 to 2015 and the Effects on Soybean Yields

Management of the soybean cyst nematode (SCN) relies heavily on use of SCN-resistant soybean varieties to limit nematode reproduction and minimize yield loss. For Iowa, almost all SCN-resistant soybean varieties contain SCN resistance genes from a breeding line named Plant Introduction (PI) 88788. Iowa State University conducts experiments to evaluate numerous SCN-resistant and three to four SCN-susceptible soybean varieties in up to nine field experiments across Iowa each year. Data on SCN population density, virulence (SCN race and HG type), soybean yield, precipitation, and growing degree days from more than 25,000 four-row plots in field experiments conducted from 2001 to 2015 were analyzed to determine how these factors affected SCN reproduction and yield. SCN population densities were positively correlated with temperatures and negatively associated with precipitation during the growing seasons, indicating that SCN reproduction was greatest in hot, dry years. Over the years, virulence of SCN populations on PI 88788 increased in the fields in which the experiments were conducted, resulting in increased end-of-season SCN population densities and reduced yields of SCN-resistant soybean varieties with the PI 88788 source of resistance. These results indicate that soybean yield loss caused by SCN on resistant varieties with the common PI 88788 source of resistance likely will increase as virulence of SCN populations increases unless new sources of resistance become widely available and used in the future.