Resistance Gene Pyramiding and Rotation to Combat Widespread Soybean Cyst Nematode Virulence

Soybean cyst nematode (SCN) is an important pathogen of soybean causing more than $1 billion in yield losses annually in the United States. Planting SCN resistant soybean cultivars is the primary management strategy. Resistance genes derived from the plant introductions (PI) 88788 (rhg1-b) and PI 548402 (Peking; rhg1-a and Rhg4) are the main types of resistance available in commercial cultivars. The PI 88788 rhg1-b resistance allele is found in the majority of SCN resistant cultivars in the north central US. The widespread use of PI 88788 rhg1-b has led to limited options for farmers to rotate resistance sources to manage SCN. Consequently, an over reliance on a single type of resistance has resulted in the selection of SCN populations that have adapted to reproduce on these resistant cultivars. Here we evaluated the effectiveness of rotating soybean lines with different combinations of resistance genes to determine the best strategy for combating the widespread increase in virulent SCN and limit future nematode adaptation to resistant cultivars. Eight SCN populations were developed by either continuous selection of a virulent SCN field population (HG type 1.2.5.7) on a single resistance source or in rotation with soybean pyramiding different resistance gene alleles derived from PI 88788 (rhg1-b), PI 437654 (rhg1-a and Rhg4), PI 468916 (cqSCN-006 and cqSCN-007) and PI 567516C (Chr10). SCN population densities were determined for eight generations. HG type tests were conducted after the eighth generation to evaluate population shifts. The continued use of rhg1-b or 006/007 had limited effectiveness for reducing SCN type 1.2.5.7 population density, whereas rotation to the use of rhg1-a/Rhg4 resistance significantly reduced SCN population density, but selected for broader SCN virulence (HG type 1.2.3.5.6.7). A rotation of rhg1-a/Rhg4 with a pyramid of rhg1-b/006/007/Chr10 was the most effective combination at both reducing population density and minimizing selection pressure. Our results provide guidance for implementation of a strategic SCN resistance rotation plan to manage the widespread virulence on PI 88788 and sustain the future durability of SCN resistance genes.

Genomic Profiling of Virulence in the Soybean Cyst Nematode Using Single-Nematode Sequencing

Soybean cyst nematode (SCN) is one of the most important diseases in soybean. Currently, the main management strategy relies on planting resistant cultivars. However, the overuse of a single resistance source has led to the selection of virulent SCN populations, although the mechanisms by which the nematode overcomes the resistance genes remain unknown. In this study, we used a nematode-adapted single-cell RNA-seq approach to identify SCN genes potentially involved in resistance breakdown in Peking and PI 88788 parental soybean lines. We established for the first time the full transcriptome of single SCN individuals allowing us to identify a list of putative virulence genes against both major SCN resistance sources. Our analysis identified 48 differentially expressed putative effectors (secreted proteins required for infection) alongside 40 effectors showing evidence of novel structural variants, and 11 effector genes containing phenotype-specific sequence polymorphisms. Additionally, a differential expression analysis revealed an interesting phenomenon of coexpressed gene regions with some containing putative effectors. The selection of virulent SCN individuals on Peking resulted in a profoundly altered transcriptome, especially for genes known to be involved in parasitism. Several sequence polymorphisms were also specific to these virulent nematodes and could potentially play a role in the acquisition of nematode virulence. On the other hand, the transcriptome of virulent individuals on PI 88788 was very similar to avirulent ones with the exception of a few genes, which suggest a distinct virulence strategy to Peking.

Dynamics of Population Density and Virulence Phenotype of the Soybean Cyst Nematode as Influenced by Resistance Source Sequence and Tillage

The soybean cyst nematode (SCN), Heterodera glycines, is the most damaging pathogen of soybean. Use of resistant cultivars is an effective strategy to manage SCN, but it also selects for virulent populations over time. A 12-year field experiment was initiated in 2003 to study how tillage and 11 different sequences of four cultivars impact SCN population dynamics and virulence. An SCN-susceptible cultivar and three resistant cultivars (R1, R2, and R3 derived from cultivars PI 88788, Peking, and PI 437654, respectively) were used. Tillage had minimal effect on SCN population density. Compared with no till, conventional tillage resulted in a faster increase of SCN virulence to Peking when the SCN was selected by R2 and virulence to PI 88788 by R3. Among the three SCN-resistant cultivars, R1 supported the greatest population density, R2 supported intermediate population density, and R3 supported the least SCN population density. The SCN populations selected by R1 overcame the resistance in PI 88788 but not in Peking and PI 437654. R2 selected SCN populations that overcame the resistance in Peking but not in PI 88788 and PI 437654. In contrast, R3 selected SCN populations that overcame both PI 88788 and Peking sources of resistance. There was no increase of virulence to PI 437654 in any cultivar sequence. R1 in rotation with R2 or R3 had a negative effect on female index on Peking. Susceptible soybean reduced SCN virulence to Peking, indicating that there was fitness cost of the Peking virulent SCN type. These results suggest that rotation of Peking with PI 88788 is a good strategy for managing the SCN, and susceptible cultivar and no till may reduce SCN virulence selection pressure in some rotations. [Formula: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .

Survey of Heterodera glycines Population Densities and Virulence Phenotypes During 2015–2016 in Missouri

The soybean cyst nematode (SCN), Heterodera glycines, is one of the most important pathogens of soybean. Periodic monitoring of SCN population densities and virulence phenotypes is necessary for developing management strategies utilizing resistant cultivars, the primary strategy used to combat this pest. Therefore, we conducted a statewide survey of Missouri to determine SCN population densities and virulence phenotypes during 2015–2016 and compared these results with a similar survey conducted in 2005. SCN population densities were determined for 393 soil samples representing 74 soybean-producing counties across eight geographical regions of Missouri. Eighty-eight percent of samples tested positive for SCN, up from 50% in 2005, and population densities ranged from 125 to 99,000 eggs per 250 cm3 of soil. The virulence phenotypes of 48 SCN populations also were determined. For this, female indices (FI) were calculated by dividing the mean number of females that develop on the roots of a set of resistant soybean indicator lines by the mean number of females that develop on the roots of susceptible cultivar Lee74 after 30 days in the greenhouse then multiplying by 100 to obtain a percentage. Notably, all SCN populations evaluated during 2015–2016 had a FI > 10 on PI 88788, the most widely used source of resistance in Missouri, in contrast to 78% in 2005. Moreover, 50% of these populations had a FI > 50 on PI 88788, up from 16% in 2005. Forty-three percent of populations tested also had a FI > 10 on Peking, the second most common source of resistance by farmers. Our results show that over the last decade, SCN has become more prevalent in Missouri fields. Additionally, the percentage of individuals within SCN field populations that are virulent on PI 88788 and Peking has markedly increased. The results stress the importance of rotating cultivars with different types of resistance when using resistant cultivars to manage SCN.

Effect of Soybean Cyst Nematode Resistance Source and Seed Treatment on Population Densities of Heterodera glycines, Sudden Death Syndrome, and Yield of Soybean

A three-year study was conducted in Illinois, Indiana, Iowa, Michigan, and Ontario, Canada, from 2013 through 2015 to determine the effect of soybean (Glycine max) cultivars’ source of soybean cyst nematode (SCN; Heterodera glycines) resistance on SCN population densities, sudden death syndrome (SDS; caused by Fusarium virguliforme), and yield of soybean. Five cultivars were evaluated with and without fluopyram seed treatment at each location. Cultivars with no SCN resistance had greater SDS severity, greater postharvest SCN egg counts (Pf), and lower yield than cultivars with plant introduction (PI) 548402 (Peking) and PI 88788-type of SCN resistance (P < 0.05). Cultivars with Peking-type resistance had lower Pf than those with PI 888788-type and no SCN resistance. In two locations with HG type 1.2-, cultivars with Peking-type resistance had greater foliar disease index (FDX) than cultivars with PI 88788-type. Fluopyram seed treatment reduced SDS and improved yield compared with a base seed treatment but did not affect SCN reproduction and Pf (P > 0.05). FDX and Pf were positively correlated in all three years (P < 0.01). Our results indicate that SDS severity may be influenced by SCN population density and HG type, which are important to consider when selecting cultivars for SCN management.

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.

Determination of Heterodera glycines Virulence Phenotypes Occurring in South Dakota

The soybean cyst nematode (SCN), Heterodera glycines, is the most important yield-limiting pathogen of soybean in the United States. In South Dakota, SCN has been found in 29 counties, as of 2016, and continues to spread. Determining the virulence phenotypes (HG types) of the SCN populations can reveal the diversity of the SCN populations and the sources of resistance that would be most effective for SCN management. To determine the HG types prevalent in South Dakota, 250 soil samples were collected from at least three arbitrarily selected fields in each of the 28 counties with fields previously found to be infested with SCN. SCN was detected in 82 fields (33%), and combined egg and juvenile counts ranged from 200 to 65,200 per 100 cm3 of soil. Eggs and juveniles were extracted from each soil sample and were used to infest seven SCN HG type test indicator soybean lines and ‘Williams 82’ as the susceptible check. A female index (FI) was calculated based on the number of females found on each indicator line relative to those on the susceptible check. A FI equal to or greater than 10% in any line was assigned as that HG type. Out of 73 SCN populations for which HG type tests were done, 63% had FI ≥10% on PI 548316 (indicator line #7), 25% on PI 88788 (#2), 19% on PI 209332 (#5), 7% on PI 548402 (#1), 4% on PI 90736 (#3), and 4% on PI 89722 (#6). None of the SCN populations had FI ≥10% on PI 437654 (indicator line #4). The most prevalent HG types were 0, 2.5.7, and 7. These accounted for 81% of all the HG types determined for the samples tested. HG types with ≥10% reproduction on indicator lines PI 88788, PI 209332, and PI 548317 were most prevalent in the soil samples tested, suggesting that the use of these sources of resistance for developing SCN resistant cultivars should be avoided. For sustainable SCN management, use of resistant cultivars should be rotated with nonhost crops and cultivars with different sources of resistance.