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).     

Field‐level effects of preventative management tactics on soybean aphids (Aphis glycines Matsumura) and their predators

A 2‐year field experiment was conducted in northern Illinois to evaluate the effects of host plant resistance and an insecticidal seed treatment (thiamethoxam) on soybean aphids, Aphis glycines Matsumura and their predators. Densities of soybean aphids varied between the 2 years of the experiment. During both years, resistant plants experienced fewer cumulative aphid days than susceptible plants. Populations of soybean aphids on resistant plants rarely exceeded the economic injury level of 250 soybean aphids per plant. The use of thiamethoxam reduced cumulative aphid days in 2007, but not in 2008. Although soybean aphids reached densities that were sufficient to cause yield‐loss for untreated and susceptible plants, no yield‐benefit was associated with using the two management tactics in either year. This latter finding suggests that densities of soybean aphids need to be greater and sustained for a longer period of time than what we observed if the two management tactics are expected to provide a yield‐benefit. Monitoring natural enemies revealed that densities of key aphidophagous predators were relatively unaffected by host plant resistance or thiamethoxam; the effect of these management tactics on densities of predators, as well as the effectiveness of the method used to sample predators, is discussed.     

Soybean aphid and soybean cyst nematode interactions in the field and effects on soybean yield

How above- and belowground plant pests interact with each other and how these interactions affect productivity is a relatively understudied aspect of crop production. Soybean cyst nematode, Heterodera glycines Ichinohe, a root parasite of soybean, Glycine max (L.) Merr., is the most threatening pathogen in soybean production and soybean aphid, Aphis glycines Matsumura, an aboveground phloem-feeding insect that appeared in North America in 2000, is the key aboveground herbivore of soybean in the midwestern United States. Now, both soybean aphid and soybean cyst nematode co-occur in soybean-growing areas in the Upper Midwest. The objectives of this study were to examine aphid colonization patterns and population growth on soybean across a natural gradient of nematode density (range, approximately 900 and 27,000 eggs per 100 cm3 soil), and to investigate the effect of this pest complex on soybean productivity. Alate (winged) soybean aphid colonization of soybean was negatively correlated to soybean cyst nematode egg density (r = -0.363, P = 0.0095) at the end of July, at the onset of peak alate colonization. However, both a manipulative cage study and openly colonized plants showed that soybean cyst nematode density below ground was unrelated to variation in aphid population growth (r approximately -0.01). Based on regression analyses, soybean aphids and cyst nematodes had independent effects on soybean yield through effects on different yield components. High soybean cyst nematode density was associated with a decline in soybean yield (kg ha(-1)), whereas increasing soybean aphid density (both alate and apterous) significantly decreased seed weight (g 100 seeds(-1)).     

Combined effects of host-plant resistance and intraguild predation on the soybean aphid parasitoid Binodoxys communis in the field

Soybean varieties that exhibit resistance to the soybean aphid Aphis glycines have been developed for use in North America. In principle, host-plant resistance to soybean aphid can influence the interactions between the soybean aphid and its natural enemies. Resistance could change the quality of soybean aphids as a food source, the availability of soybean aphids, or resistance traits could directly affect aphid predators and parasitoids. Here, we focus on the effect of soybean aphid resistance on the interactions between soybean aphids, the parasitoid Binodoxys communis (Hymenoptera: Braconidae), and predators of these two species. We determined whether host-plant resistance affected within-season persistence of B. communis by releasing parasitoids into resistant and susceptible soybean plots. We observed higher B. communis densities in susceptible soybean plots than in resistant plots. There were also higher overall levels of intraguild predation of B. communis in susceptible plots, although the per-capita risk of intraguild predation of B. communis was affected neither by plant genotype nor by aphid density. We discuss these effects and whether they were caused by direct effects of the resistant plants on B. communis or indirect effects through soybean aphid or predators.     

Biological control potential of plant growth‐promoting rhizobacteria suppression of Meloidogyne incognita on cotton and Heterodera glycines on soybean: A review

Over the past decade, we have seen an increasing market for biopesticides and an increase in number of microbial control studies directed towards plant‐parasitic nematodes. This literature survey provides an overview of research on biological control of two economically important plant‐parasitic nematodes, Meloidogyne incognita (Kofoid & White) Chitwood (southern root‐knot nematode) and Heterodera glycines Ichinohe (soybean cyst nematode) using spore‐forming plant growth‐promoting rhizobacteria (PGPR). In this review, the current biological control strategies for the management of those cotton and soybean nematodes, the mechanism of using BacillusPGPR for biological control of plant‐parasitic nematode including induced systemic resistance and antagonism and the future of biological control agents on management of plant‐parasitic nematodes are covered.     

Manipulation of two α‐endo‐β‐1,4‐glucanase genes,AtCel6 and GmCel7, reduces susceptibility to Heterodera glycines in soybean roots

Plant endo‐β‐1,4‐glucanases (EGases) include cell wall‐modifying enzymes that are involved in nematode‐induced growth of syncytia (feeding structures) in nematode‐infected roots. EGases in the α‐ and β‐subfamilies contain signal peptides and are secreted, whereas those in the γ‐subfamily have a membrane‐anchoring domain and are not secreted. The Arabidopsis α‐EGase At1g48930, designated as AtCel6, is known to be down‐regulated by beet cyst nematode (Heterodera schachtii) in Arabidopsis roots, whereas another α‐EGase, AtCel2, is up‐regulated. Here, we report that the ectopic expression of AtCel6 in soybean roots reduces susceptibility to both soybean cyst nematode (SCN; Heterodera glycines) and root knot nematode (Meloidogyne incognita). Suppression of GmCel7, the soybean homologue of AtCel2, in soybean roots also reduces the susceptibility to SCN. In contrast, in studies on two γ‐EGases, both ectopic expression of AtKOR2 in soybean roots and suppression of the soybean homologue of AtKOR3 had no significant effect on SCN parasitism. Our results suggest that secreted α‐EGases are likely to be more useful than membrane‐bound γ‐EGases in the development of an SCN‐resistant soybean through gene manipulation. Furthermore, this study provides evidence that Arabidopsis shares molecular events of cyst nematode parasitism with soybean, and confirms the suitability of the Arabidopsis–H. schachtii interaction as a model for the soybean–H. glycines pathosystem.     

Two‐year oscillation cycle in abundance of soybean aphid in Indiana

• 1 The present study evaluated the population dynamics of the heteroecious soybean aphid Aphis glycines Matsumura (Hemiptera: Aphididae) during an 8‐year period in Indiana, shortly after its detection in North America. Sampling conducted at multiple locations revealed that A. glycines exhibited a 2‐year oscillation cycle that repeated itself four times between 2001 and 2008: years of low aphid abundance were consistently followed by years of high aphid abundance.
• 2 Similar patterns of abundance of A. glycines and coccinellids (Coleoptera: Coccinellidae) in soybean fields, both within and between‐years, suggest that late season predation by coccinellids plays a role in the oscillatory cycle of aphids. Insidious flower bugs Orius insidiosus (Say) (Hemiptera: Anthocoridae) were numerically more abundant than coccinellids, although the lack of synchrony between aphids and predatory bugs suggests that O. insidiosus has a limited influence on between‐year variations in aphid density.
• 3 The inverse relationship between aphid densities before and after the start of the autumn migratory period changes direction in alternate years. High aphid density on soybean in the summer is associated with a reduced number of alate migrants produced in the autumn. Conversely, years with low density aphids on soybean in the summer are characterized by high numbers of alates that migrate to the primary host in the autumn.
• 4 From a pest management perspective, the 2‐year oscillation cycle of A. glycines is a desirable attribute with respect to population dynamics because it implies that aphids cause significant economic damage only in alternate years (as opposed to every year). Cultural practices enhancing the conservation biological control of Coccinellidae may help to preserve the periodicity of aphid infestation and restrict the pest status of A. glycines.

     

Performance and prospects of Rag genes for management of soybean aphid

The soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is an invasive insect pest of soybean [Glycine max (L.) Merr. (Fabaceae)] in North America, and it has led to extensive insecticide use in northern soybean‐growing regions there. Host plant resistance is one potential alternative strategy for managing soybean aphid. Several Rag genes that show antibiosis and antixenosis to soybean aphid have been recently identified in soybean, and field‐testing and commercial release of resistant soybean lines have followed. In this article, we review results of field tests with soybean lines containing Rag genes in North America, then present results from a coordinated regional test across several field sites in the north‐central USA, and finally discuss prospects for use of Rag genes to manage soybean aphids. Field tests conducted independently at multiple sites showed that soybean aphid populations peaked in late summer on lines with Rag1 or Rag2 and reached economically injurious levels on susceptible lines, whereas lines with a pyramid of Rag1 + Rag2 held soybean aphid populations below economic levels. In the regional test, aphid populations were generally suppressed by lines containing one of the Rag genes. Aphids reached putative economic levels on Rag1 lines for some site years, but yield loss was moderated, indicating that Rag1 may confer tolerance to soybean aphid in addition to antibiosis and antixenosis. Moreover, no yield penalty has been found for lines with Rag1, Rag2, or pyramids. Results suggest that use of aphid‐resistant soybean lines with Rag genes may be viable for managing soybean aphids. However, virulent biotypes of soybean aphid were identified before release of aphid‐resistant soybean, and thus a strategy for optimal deployment of aphid‐resistant soybean is needed to ensure sustainability of this technology.     

Linkage of soybean cyst nematode alleles for incompatibility with soybean

Selection and inbreeding of soybean cyst nematodes increased populations' ability to produce cysts on some soybean lines with concurrent decreases in numbers of cysts on other soybean lines: evidence that some alleles for incompatibility were either linked or at the same loci. Some responses could be explained only by linkage of nematode genes for avirulence. Linkage of nematode alleles for incompatibility could be involved when selection increased numbers of cysts on several lines even though the usual interpretation has been that the lines had some of the same genes for resistance. Most of the lines used in this study may have fewer alleles for incompatibility than most "resistant" lines. Use of these lines with fewer genes for resistance should help in the identification of individual alleles for incompatibility necessary for resolving the allelism and/or linkage of these nematode genes.     

Temperature influences the expression of resistance of soybean (Glycine max) to the soybean aphid (Aphis glycines)

Resistance of plants to arthropods may be lost at low or high temperatures. I tested whether the relative resistance of five genotypes of soybean, Glycine max (L.) Merr., to three isolates of the soybean aphid, Aphis glycines Matsumura, was influenced by three temperatures, 14, 21 and 28°C, in no‐choice tests in the laboratory. The interaction between temperature and the genotype of soybean influenced the population sizes of two isolates of A. glycines. Two genotypes of soybean, LD05‐16611 and PI 567597C, which usually are resistant to isolate 1 and 3, became susceptible: LD05‐16611 at the low temperature and PI 567597C at the high temperature. The genotypes PI 200538 and PI 567541B usually are susceptible to isolate 3 but were resistant at 21 and 28°C. I can only speculate as to the reason why temperature influences resistance of some genotypes of soybean to A. glycines: A. glycines may be directly influenced by temperature or indirectly influenced by changes in the host plant. Nevertheless, my results suggest that temperature may be one factor that influences the expression of resistance of soybean to A. glycines, so genotypes of soybean should be screened for resistance to the aphid at multiple temperatures.     

Selection of nematodes for zero cyst phenotypes with soybean

Definitive genetic studies of the soybean cyst nematode (Heterodera glycines)-soybean (Glycine max) relationship are complicated by the use of soybean lines with many genes for resistance to heterogeneous, amphimictic nematode populations. Inbreeding and artificial selection of cyst nematodes decreased their ability to form cysts on specific soybean lines assumed to have few genes for resistance. In the initial sib selection, single cysts were used to inoculate two-seedling units consisting of a seedling of one soybean line to evaluate the nematodes' ability to form cysts on it and a seedling of another line for comparison and maintenance of the nematode inbreds being developed. This method permitted some selection but was slow and labour-intensive. A better method of artificial selection for fewer cysts on specific soybean lines was to inbreed nematodes for about four generations, then to evaluate the inbreds for ability to form cysts on the soybean lines before selecting particular inbreds with poor ability to form cysts for the development of more inbreds. This increased the frequencies of specific nematode genes for avirulence or alleles for incompatibility with soybean lines containing the interacting [gene-for-gene] alleles for incompatibility (genes for resistance). The artificial selection apparently was for at least two nematode alleles for incompatibility since at least two soybean alleles were indicated in the segregation from crosses of soybean lines.     

Impact of Herbicides on Heterodera glycines Susceptible and Resistant Soybean Cultivars

Several abiotic and biotic stresses can affect soybean in a growing season. Heterodera glycines, soybean cyst nematode, reduces yield of soybean more than any other pathogen in the United States. Field and greenhouse studies were conducted to determine whether preemergence and postemergence herbicides modified the reproduction of H. glycines, and to determine the effects of possible interactive stresses caused by herbicides and H. glycines on soybean growth and yield. Heterodera glycines reproduction factor (Rf) generally was less on resistant than susceptible cultivars, resulting in a yield advantage for resistant cultivars. The yield advantage of resistant cultivars was due to more pods per plant on resistant than susceptible cultivars. Pendimethalin reduced H. glycines Rf on the susceptible cultivars in 1998 at Champaign, Illinois, and in greenhouse studies reduced dry root weight of H. glycines-resistant and susceptible cultivars, therefore reducing Rf on the susceptible cultivars. The interactive stresses from acifluorfen or imazethapyr and H. glycines reduced the dry shoot weight of the resistant cultivar Jack in a greenhouse study. Herbicides did not affect resistant cultivars'' ability to suppress H. glycines Rf; therefore, growers planting resistant cultivars should make herbicide decisions based on weeds present and cultivar tolerance to the herbicide.     

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.     

Effects of Rag1 aphid‐resistant soybean on mortality,development, and preference of brown marmorated stink bug

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), poses a new threat to soybean, Glycine max (L.) Merrill (Fabaceae), production in the north central USA. As H. halys continues to spread and increase in abundance in the region, the interaction between H. halys and management tactics deployed for other pests must be determined. Currently, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), is the most abundant and damaging insect pest of soybean in the region. Aphid‐resistant soybean, mainly with the Rag1 gene, is commercially available for management of A. glycines. Here, experiments were performed to evaluate the effects of Rag1 aphid‐resistant soybean on the mortality, development, and preference of H. halys. In a no‐choice test, mortality of H. halys reared on Rag1 aphid‐resistant soybean pods was significantly lower than when reared on aphid‐susceptible soybean pods (28 vs. 53%). Development time, adult weight, and proportion females of surviving adults did not differ when reared on Rag1 aphid‐resistant or aphid‐susceptible soybean pods. In choice tests, H. halys exhibited a preference for Rag1 aphid‐resistant over aphid‐susceptible soybean pods after 4 h, but not after 24 h. Halyomorpha halys exhibited no preference when tested with vegetative‐stage or reproductive‐stage soybean plants. The preference by H. halys for Rag1 aphid‐resistant soybean pods and the decreased mortality when reared on these pods suggests that the use of Rag1 aphid‐resistant soybean may favor this emerging pest in the north central USA.     

Development of methods to evaluate susceptibility of soybean aphid to imidacloprid and thiamethoxam at lethal and sublethal concentrations

The soybean aphid, Aphis glycines Matsumura (Homoptera: Aphididae), is a recent introduction (2000) from Asia and has become a serious soybean [Glycine max (L.) Merr. (Fabaceae)] pest in North America. Seed treatments using the neonicotinoid insecticides, imidacloprid and thiamethoxam, have been suggested as a method of control, and the use of these insecticides is becoming widespread. As a consequence, there is increased potential to select for resistance to these compounds. In the case of soybean aphids, baseline susceptibility to neonicotinoid insecticides and standardized methods for bioassay are lacking. A bioassay technique that uses excised soybean leaves immersed in an insecticide solution was developed to determine systemic insecticidal activity at lethal and sublethal concentrations. Mortality and population growth inhibition were evaluated after 7 days. Life table parameters were calculated by exposing 1‐day‐old aphids to three concentrations of thiamethoxam. Aphid mortality and nymph production were recorded daily until the entire cohort collapsed. Soybean aphid age‐specific survivorship, fecundity, net reproductive rate, longevity, intrinsic rate of increase, discrete daily growth rate, and life expectancy were all significantly reduced at higher thiamethoxam concentrations. Soybean aphid response to both insecticides was similar, and both compounds were very toxic with LC₅₀s of 31.3 and 16.9 ng ml^?1 and EC₅₀s of 6.3 and 5.4 ng ml^?1 for imidacloprid and thiamethoxam, respectively. These results indicate that the methods developed in this study had negligible impact on the life table estimates measured and can be used to develop a baseline of susceptibility as a benchmark for subsequent resistance monitoring. Given the rapid and widespread adoption of this new insecticide class, vigilant monitoring for changes in susceptibility will be essential to its long‐term sustainability.     

A recessive soybean cyst nematode allele for incompatibility with soybean PI 88287

The objective of this research was to characterise the degree of dominance of a soybean cyst nematode (Heterodera glycines) allele for incompatibility which interacts with a recessive soybean (Glycine max) allele for incompatibility to prevent the formation of cysts. Crosses of inbred nematode populations were made and the F, and F, populations evaluated for the numbers of cysts they could produce on several soybean lines. The nematode gene for avirulence interacts with the one recessive gene for resistance in soybean line PI 88287 and also appears to be recessive. This is the first example of a recessive-recessive gene-for-gene interaction; genes for avirulence and resistance are usually dominant. The difficulties of doing definitive genetic studies with cyst nematodes are discussed.     

Genetic mapping of soybean cyst nematode race-3 resistance loci in the soybean PI 437.654

Resistance to the soybean cyst nematode (SCN) (Heterodera glycines Ichinohe) is difficult to evaluate in soybean [Glycine max (L.) Merr.] breeding. PI 437.654 has resistance to more SCN race isolates than any other known soybean. We screened 298 F₆₇ recombinant-inbred lines from a cross between PI 437.654 and BSR101 for SCN race-3 resistance, genetically mapped 355 RFLP markers and the I locus, and tested these markers for association with resistance loci. The Rhg ₄ resistance locus was within 1 cM of the I locus on linkage group A. Two additional QTLs associated with SCN resistance were located within 3cM of markers on groups G and M. These two loci were not independent because 91 of 96 lines that had a resistant-parent marker type on group G also had a resistant-parent marker type on group M. Rhg ₄ and the QTL on G showed a significant interaction by together providing complete resistance to SCN race-3. Individually, the QTL on G had greater effect on resistance than did Rhg ₄, but neither locus alone provided a degree of resistance much different from the susceptible parent. The nearest markers to the mapped QTLs on groups A and G had allele frequencies from the resistant parent indicating 52 resistant lines in this population, a number not significantly different from the 55 resistant lines found. Therefore, no QTLs from PI 437.654 other than those mapped here are expected to be required for resistance to SCN race-3. All 50 lines that had the PI 437.654 marker type at the nearest marker to each of the QTLs on groups A and G were resistant to SCN race-3. We believe markers near to these QTLs can be used effectively to select for SCN race-3 resistance, thereby improving the ability to breed SCN-resistant soybean varieties.     

On‐farm evaluation of a fall‐seeded rye cover crop for suppression of soybean aphid (Hemiptera: Aphididae) on soybean

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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.