Loss of Effective Soybean Phytophthora Root and Stem Rot Resistance Genes

CPN 5014. Published June 18, 2024. Doi.org/10.31274/cpn-20240618-1.

Austin G. McCoy, Michigan State University; Richard R. Belanger Université Laval; Carl A. Bradley, University of Kentucky; Daniel G. Cerritos-Garcia, University of Connecticut; Vinicius C. Garnica, North Carolina State University; Loren J. Giesler, University of Nebraska-Lincoln; Pablo E. Grijalba, Universidad de Buenos Aires;  Eduardo Guillin, Instituto Nacional de Tecnologia Agropecuaria; Maria A. Henriquez, Agriculture and Agri-Food Canada, Morden; Yong Min Kim, Agriculture and Agri-Food Canada, Brandon; Dean K. Malvick, University of Minnesota; Rashelle L. Matthiesen, Iowa State University; Santiago X. Mideros, University of Illinois, Zachary A. Noel, Auburn University; Alison E. Robertson, Iowa State University; Mitchell G. Roth, Farmers Business Network; Clarice L. Schmidt, Iowa State University; Damon L. Smith, University of Wisconsin-Madison; Adam H. Sparks, Curtin University, Perth; Darcy E. P. Telenko, Purdue University; Vanessa Tremblay, Université Laval; Owen Wally, Agriculture and Agri-Food Canada, Harrow; Eric Anderson, Mike Staton, and Martin I. Chilvers, Michigan State University.

Summary

• Globally there has been a loss of previously effective soybean resistance genes (Rps) to Phytophthora sojae.

• Phytophthora sojae individuals (isolates) can now cause disease on more Rps resistance genes than they could 10 years ago, making disease management with Rps-genes more difficult.

• The most widely available Phytophthora root and stem rot resistance genes—Rps1a, Rps1c, Rps1k—currently only protect against 11%, 26%, and 15% of Phytophthora sojae individuals in the United States, and 2%, 16%, and 56% of individuals in Canada, respectively. However, efficacy of different Rps genes varies across states and fields.

• Rps3a currently protects against 81% of Phytophthora sojae individuals in the United States, and 90% in Canada.

• Best management practices for Phytophthora root and stem rot are to select soybean cultivars with an effective Rps-gene (such as Rps3a), moderate to high levels of partial resistance, and to apply an effective seed treatment containing metalaxyl/mefenoxam, ethaboxam, oxathiapiprolin, or picarbutrazox.

Introduction

Phytophthora root and stem rot (PRSR) of soybean is caused by Phytophthora sojae, which is an oomycete (a.k.a. water mold – not a fungus). Phytophthora root and stem rot is a prevalent disease in all soybean producing regions. The pathogen can survive in the soil as resting spores called oospores for many years. Under favorable conditions such as saturated soils, these oospores germinate to produce sporangia which release zoospores that swim toward and infect soybean roots. Soybean plants will typically start showing symptoms in mid- to late-July, but PRSR can occur at any time of the year after periods of warm (at least 70 F or 21 C) and wet weather (Dorrance 2018). Climate models suggest that instances of intense rain and saturated soils will likely become more frequent in the coming years, providing more favorable conditions for Phytophthora diseases (Konapala et al. 2020).

The use of resistant soybean cultivars is one of the most effective disease management tools. There are two forms of resistance to Phytophthora within soybean cultivars: resistance genes to P. sojae (Rps); and partial resistance, which may be referred to as field tolerance in seed catalogues. In seed catalogues, soybean cultivars known to contain Rps genes may be labeled as such, for example “contains Rps1c gene.” Effective Rps resistance genes confer complete protection from P. sojae populations that cannot overcome those genes. Partial resistance will not confer complete protection but will reduce disease severity and yield loss when under PRSR pressure. However, partial resistance is not active until the first trifoliate leaves are formed, so seed treatments should be used to protect seedlings early in the season. Fungicide seed treatments with efficacy against P. sojae can help reduce seedling disease for a couple of weeks following planting but will not protect plants for the entire season.

Recent surveys within the United States, Canada, and Argentina suggested that P. sojae populations, or a collection of P. sojae individuals, were overcoming the Rps1c and Rps1k sources of resistance in many areas, but no country-wide or global study on the efficacy of these resistance genes had been performed. Our objectives were to determine if P. sojae populations were adapting to, and able to cause disease on, widely used Rps genes on a national and global scale in the United States, Canada, Argentina, and China.

Research Goals

• Determine which soybean Rps genes are effective for management of Phytophthora root and stem rot

• Identify the extent of P. sojae populations adaptation to Rps genes by evaluating pathotype complexity over time

• Evaluate the efficacy of tested Rps genes on a country-wide and global scale

• Determine how the diversity of P. sojae pathotypes has changed due to adaptation to Rps genes over time

The Research

Recent PRSR outbreaks and subsequent P. sojae surveys conducted by extension pathologists question the current state of Rps gene efficacy in disease management. However, a worldwide analysis of Rps gene efficacy has not been conducted. Therefore, a global collaboration of plant pathologists led by Michigan State University was initiated to identify the current state of Rps gene efficacy on a national and global scale. We analyzed Phytophthora sojae survey work conducted by plant pathologists around the world from the last 30 years, representing Rps gene efficacy data on over 5,000 P. sojae individuals, 29 published studies, and data from the United States, Canada, Argentina and China. We found that the most common resistance genes—Rps1a, Rps1c, and Rps1k—are no longer widely effective in the United States, Canada, and Argentina. As any given soybean field contains a diverse population of P. sojae individuals capable of causing disease on plants with different Rps genes, it is important to utilize genes that control most individuals within a field. This study also showed that individuals of P. sojae are now more complex, that is, each individual is able to cause disease on more Rps genes than they were 10 years ago.

In the United States, Canada, and Argentina Rps1a, Rps1c, and Rps1k are the most readily available Rps genes available in commercial soybean cultivars for farmers to utilize. In the United States and Canada, soybean cultivars with the Rps3a gene are available but only in a few cultivars.  

In the United States, the majority of widely deployed Rps genes only control a fraction of the P. sojae individuals (Figure 2); Rps1a, Rps1c and Rps1k controlled 11%, 26% and 15% of P. sojae individuals, respectively. Only one Rps gene available to farmers for PRSR management was found to be widely effective the United States: Rps3a which controlled 81% of P. sojae individuals. A similar trend was also found in Canada (Figure 2). An increase in availability of effective Rps genes, such as Rps3a, will be needed from companies to effectively manage PRSR in the future. In the meantime, farmers with fields that have a history of PRSR can use soybean cultivars with the Rps3a gene and moderate to high levels of partial resistance in combination with an effective fungicide seed treatment to protect yield.

Conclusions

The P. sojae populations in the United States, Argentina, and Canada have adapted in many areas to the most-deployed Rps genes for controlling PRSR: Rps1a, Rps1c, and Rps1k. Consequently, individuals of P. sojae in these countries can currently overcome 1 to 3 more Rps genes than they could 10 to 30 years ago. Phytophthora sojae pathotypes continue to become more diverse but are now predominantly able to overcome the Rps1c and Rps1k genes. The Rps genes, Rps3a and Rps6, both appear to be widely effective in the United States, Canada, and Argentina but would need to be widely deployed commercially to benefit farmers in managing PRSR of soybean. However, widespread use of Rps3a and Rps6, will likely impose additional selection pressure on the P. sojae population causing it to also evolve resistance to these two genes. Consequently, Rps3a and Rps6 should be deployed in combination with a background of high partial resistance, and an effective fungicide seed treatment to reduce resistance developing.

This research update is based on the work described in the following peer-reviewed research article and adapted from a Michigan State University Extension article:

McCoy, A. G., Belanger, R. R., Bradley, C. A., Cerritos-Garcia, D. G., Garnica, V. C., Geisler, L. J., Grijalba, P. E., Guillin, E., Henriquez, M. A., Kim, Y. M., Malvick, D. K., Matthiesen, R. L., Mideros, S. X., Noel, Z. A., Robertson, A. E., Roth, M. G., Schmidt, C. L., Smith, D. L., Sparks, A. H., Telenko, D. E. P., Tremblay, V., Wally, O., Chilvers, M. I. 2023. A global-temporal analysis on Phytophthora sojae resistance-gene efficacy. Nature Communications 14:6043. Article / Google Scholar

McCoy, A., Chilvers, M., Anderson, E., and Staton, M. 2023. Soybean Phytophthora stem and root rot resistance genes have become less effective. Michigan State University Extension. Article

References

Konapala, G., Mishra, A. K., Wada, Y., and Mann, M. E. 2020. Climate change will affect global water availability through compounding changes in seasonal precipitation and evaporation. Nat. Commun. 11:1–10. Article / Google Scholar

Dorrance, A. E. 2018. Management of Phytophthora sojae of soybean: a review and future perspectives. Can. J. Plant Pathol. 40:210–219 (2018). Article / Google Scholar

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Acknowledgements

This work was made possible by partial support from Michigan Soybean Committee, Project GREEEN, North Central Soybean Research Program, and the United Soybean Board.

Authors

Austin G. McCoy, Michigan State University; Richard R. Belanger, Université Laval; Carl A. Bradley, University of Kentucky; Daniel G. Cerritos-Garcia, University of Connecticut; Vinicius C. Garnica, North Carolina State University; Loren J. Giesler, University of Nebraska-Lincoln; Pablo E. Grijalba, Universidad de Buenos Aires;  Eduardo Guillin, Instituto Nacional de Tecnologia Agropecuaria; Maria A. Henriquez, Agriculture and Agri-Food Canada, Morden; Yong Min Kim, Agriculture and Agri-Food Canada, Brandon; Dean K. Malvick, University of Minnesota; Rashelle L. Matthiesen, Iowa State University; Santiago X. Mideros, University of Illinois, Zachary A. Noel, Auburn University; Alison E. Robertson, Iowa State University; Mitchell G. Roth, Farmers Business Network; Clarice L. Schmidt, Iowa State University; Damon L. Smith, University of Wisconsin-Madison; Adam H. Sparks, Curtin University, Perth; Darcy E. P. Telenko, Purdue University; Vanessa Tremblay, Université Laval; Owen Wally, Agriculture and Agri-Food Canada, Harrow; Eric Anderson, Mike Staton, and Martin I. Chilvers, Michigan State University.

Reviewers

Travis Faske, University of Arkansas and Daren Mueller, Iowa State University.