Monitoring for resistance to the SDHI fungicide seed treatments ILEVO (fluopyram) and Saltro (pydiflumetofen) for soybean sudden death syndrome (SDS) management

Ryan Hamilton, Michigan State University; Janette L. Jacobs, Michigan State University; Austin G. McCoy, Michigan State University; Heather M. Kelly, University of Tennessee Institute of Agriculture; Carl A. Bradley, University of Kentucky; Dean K. Malvick, University of Minnesota, J. Alejandro Rojas, Michigan State University, and Martin I. Chilvers, Michigan State University. 

Summary

• The objective of this study was to look for evidence of fungicide resistance development in Fusarium virguliforme, the causal fungus of sudden death syndrome (SDS), to the fungicides used for SDS management: fluopyram (ILEVO) and pydiflumetofen (Saltro) in a series of laboratory experiments.

• There is no evidence of fluopyram (ILEVO) resistance occurrence in F. virguliforme: Among the F. virguliforme samples from the U.S. tested in this study, there was no change in fluopyram sensitivity between 2006 and 2022. 

• Fluopyram (ILEVO) and pydiflumetofen (Saltro) sensitivity in F. virguliforme are correlated: As sensitivity to fluopyram changes, the sensitivity to pydiflumetofen changes proportionally.

• Rotating between fluopyram (ILEVO) and pydiflumetofen (Saltro) is not an effective fungicide resistance management strategy: Both active ingredients have the same mode of action (FRAC 7), so switching between them will not avoid SDHI fungicide resistance development.

• Action items: In fields with a high risk for SDS, it is important to pair soybean variety resistance with an effective seed treatment. Report suspected fungicide failures to your university extension contact to aid in monitoring for fungicide resistance. 

Introduction 

Sudden death syndrome (SDS) is consistently among the most important yield-limiting diseases of soybean in North America, with estimated yield losses over 23 million bushels, amounting to approximately $300 million USD in 2023 (CPN 2024). The causal agents of soybean SDS vary between North and South America, but the primary causal agent of SDS in North America is the soil dwelling fungal pathogen, Fusarium virguliforme (Aoki et al. 2003; O’Donnell et al. 2010).

F. virguliforme infects soybean roots causing root rot. Though fungal growth is restricted to soybean roots, the most easily identifiable symptoms of SDS occur on leaves: interveinal chlorosis (yellowing) and necrosis (browning) (Figure 1). For more information on the SDS disease cycle and management strategies, check out the Crop Protection Network’s Overview of Sudden Death Syndrome.

Seed treatments containing the succinate dehydrogenase inhibitor (SDHI – FRAC group 7) fungicides fluopyram (labeled as ILEVO) and pydiflumetofen (labeled as Saltro) have been effective in reducing both root and foliar symptom severity and were registered for SDS management in 2014 and 2019, respectively (Kandel et al. 2023). It has been 10 years since the baseline sensitivity of F. virguliforme to fluopyram was determined and USDA approval of fluopyram for SDS management in the field (Wang et al. 2017). Additionally, the Fungicide Resistance Action Committee (FRAC) considers SDHI fungicides to be medium-to-high risk for cross-resistance development. Cross-resistance is when resistance to one fungicide also results in resistance to another fungicide, often within the same FRAC group (FRAC 2022). Therefore, early detection of resistance development in F. virguliforme is critically important to preserve the efficacy of integrated SDS management strategies. 

Research Goals 

• Determine if there has been a significant shift in fluopyram sensitivity in F. virguliforme since its approval for use in managing SDS.

• Assess pydiflumetofen sensitivity in a subset of 23 F. virguliforme samples and look for evidence of cross-resistance between fluopyram and pydiflumetofen in F. virguliforme. 

The Research 

Methods 

To accomplish the first goal, we tested 80 historical F. virguliforme samples, collected from 6 U.S. states in 2006-2013, against fluopyram in a “poison plate” assay. In this context, the poison plate assay involved growing F. virguliforme colonies in petri dishes on an artificial medium with increasing concentrations of fluopyram (Figures 2 and 3). The colony area was then measured 3- and 10-days after being placed on the fluopyram-amended medium and the average growth rate at each concentration was calculated. The difference between the fungal growth rate of colonies grown on the medium without fluopyram and the growth rate at each successive concentration of fluopyram was then used to calculate what is known as an EC₅₀ value. 

EC₅₀ refers to the effective fungicide concentration at which fungal colony growth is inhibited by 50% and is a common way to report fungicide sensitivity. The average fluopyram sensitivity (or EC₅₀) of these 80 historical samples were then compared to the fluopyram sensitivity of 123 contemporary F. virguliforme samples collected from 11 states in 2016-2022 (Figure 4).

Next, we selected 23 of these samples and tested them against pydiflumetofen using the same methods. Statistical analysis of the relationship between the average fluopyram EC₅₀ value and the average pydiflumetofen EC₅₀ value of each respective sample was conducted. The relationship (or correlation) between these two fungicide sensitivity measurements can be evidence of the potential for cross-resistance. 

Results

Among the historical F. virguliforme samples, collected between 2006-2013, it took between 1.64 mg/L and 7.30 mg/L of fluopyram to stop F. virguliforme growth by 50%, with an average EC₅₀ of 3.95 mg/L. For the contemporary samples, collected in 2016-2022, it took between 1.19 mg/L and 7.71 mg/L, with an average EC₅₀ of 4.19 mg/L.

Overall, no differences were found in how much fluopyram was needed to control F. virguliforme growth, whether the samples were older or newer (P = 0.10) or collected from different U.S. states (Figure 5).

In the F. virguliforme samples tested against pydiflumetofen, it required between 0.04 mg/L to 0.24 mg/L to inhibit fungal growth by 50%, with an average EC₅₀ of 0.11 mg/L. A positive correlation relationship, was found between the amount of fluopyram and the amount of pydiflumetofen needed for control of fungal growth in the samples tested against both fungicides (R = 0.53, P < 0.01) (Figure 6). 

Conclusions 

No difference was found between the historical and contemporary groups of F. virguliforme samples, but how does this relate to the efficacy of these fungicides in SDS management in the field? In simplest terms, both fluopyram (ILEVO) and pydiflumetofen (Saltro) are still effective fungicides to include in SDS integrated management programs. 

The relationship between fluopyram and pydiflumetofen sensitivity found in this study suggests F. virguliforme field populations that are less sensitive to fluopyram are also likely to be less sensitive to pydiflumetofen. This was expected as both fungicides are in the same FRAC group (SDHIs – FRAC group 7). Thus, switching between these two seed treatments ILEVO and Saltro is not an effective strategy to delay fungicide resistance development in F. virguliforme field populations.

Timely sensitivity monitoring is important to the early detection of fungicide resistance development. These efforts help maximize the durability of current management practices, delay fungicide resistance development in pathogen field populations, and promote good environmental stewardship through responsible use of fungicides.

In fields with a high risk for SDS, it is important to plant an SDS-resistant soybean variety with a seed treatment that is specifically labeled for SDS management. Be sure to report any suspected fungicide efficacy failures to your local university extension contact to help in monitoring for fungicide resistance. 

Find Out More

For more information on SDS management, see An Overview of Sudden Death Syndrome.

This research update summarizes the work described in the following peer-reviewed research article: 

Hamilton, R., Jacobs, J. L., McCoy, A. G., Kelly, H. M., Bradley, C., Malvick, D., J.A., Rojas, Chilvers, M.I. 2023. Multistate sensitivity monitoring of Fusarium virguliforme to the SDHI fungicides fluopyram and pydiflumetofen in the United States. Plant Disease 108:1602–1611. Article | Google Scholar 

References 

Aoki, T., O’Donnell, K., Homma, Y., and Lattanzi, A. R. 2003. Sudden-Death Syndrome of Soybean Is Caused by Two Morphologically and Phylogenetically Distinct Species within the Fusarium solani Species Complex: F. virguliforme in North America and F. tucumaniae in South America. Mycologia. 95:660–684. Article | Google Scholar

FRAC. 2022. Fungicide Resistance Action Committee (FRAC) - Recommendations for SDHI fungicides. 2022. Accessed April 30, 2023. Website

Kandel, Y. R., Lawson, M. N., Brown, M. T., Chilvers, M. I., Kleczewski, N. M., Telenko, D. E. P., et al. 2023. Field and greenhouse assessment of seed treatment fungicides for management of sudden death syndrome and yield response of soybean. Plant Disease 107:1131–1138. Accessed October 7, 2022. Article | Google Scholar

O’Donnell, K., Sink, S., Scandiani, M. M., Luque, A., Colletto, A., Biasoli, M., et al. 2010. Soybean Sudden Death Syndrome Species Diversity Within North and South America Revealed by Multilocus Genotyping. Phytopathology. 100:58–71. Article | Google Scholar

CPN. Crop Protection Network Disease Loss Calculator. 2024. Online Resource.

Wang, J., Bradley, C. A., Stenzel, O., Pedersen, D. K., Reuter-Carlson, U., and Chilvers, M. I. 2017. Baseline Sensitivity of Fusarium virguliforme to Fluopyram Fungicide. Plant Disease. 101:576–582. Article | Google Scholar

Acknowledgements 

Authors

Ryan Hamilton, Michigan State University; Janette L. Jacobs, Michigan State University; Austin G. McCoy, Michigan State University; Heather M. Kelly, University of Tennessee Institute of Agriculture; Carl A. Bradley, University of Kentucky; Dean K. Malvick, University of Minnesota, J. Alejandro Rojas, Michigan State University, and Martin I. Chilvers, Michigan State University 

Reviewers

Daren Mueller, Iowa State University; Damon Smith, University of Wisconsin-Madison; and Kiersten Wise, University of Kentucky.

The authors would like to thank the Michigan Soybean Committee, Project GREEEN, North Central Soybean Research Program, United Soybean Board, and BASF for providing support for this study.