The Response to Phakopsora Pachyrhizi (Soybean Rust) in North America Heather Y
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University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Plant Pathology Plant Pathology Department 2015 From Select Agent to an Established Pathogen: The Response to Phakopsora pachyrhizi (Soybean Rust) in North America Heather Y. Kelly University of Tennessee Nicholas S. Dufault University of Florida David R. Walker University of Illinois Scott A. Isard Louisiana State University Agricultural Center Raymond W. Schneider University of Nebraska-Lincoln See next page for additional authors Follow this and additional works at: http://digitalcommons.unl.edu/plantpathpapers Part of the Other Plant Sciences Commons, Plant Biology Commons, and the Plant Pathology Commons Kelly, Heather Y.; Dufault, Nicholas S.; Walker, David R.; Isard, Scott A.; Schneider, Raymond W.; Giesler, Loren J.; Wright, David L.; Marois, James J.; and Hartman, Glen L., "From Select Agent to an Established Pathogen: The Response to Phakopsora pachyrhizi (Soybean Rust) in North America" (2015). Papers in Plant Pathology. 320. http://digitalcommons.unl.edu/plantpathpapers/320 This Article is brought to you for free and open access by the Plant Pathology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Plant Pathology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Heather Y. Kelly, Nicholas S. Dufault, David R. Walker, Scott A. Isard, Raymond W. Schneider, Loren J. Giesler, David L. Wright, James J. Marois, and Glen L. Hartman This article is available at DigitalCommons@University of Nebraska - Lincoln: http://digitalcommons.unl.edu/plantpathpapers/320 Ecology and Epidemiology From Select Agent to an Established Pathogen: The Response to Phakopsora pachyrhizi (Soybean Rust) in North America Heather Y. Kelly, Nicholas S. Dufault, David R. Walker, Scott A. Isard, Raymond W. Schneider, Loren J. Giesler, David L. Wright, James J. Marois, and Glen L. Hartman First author: Department of Entomology and Plant Pathology, West Tennessee Research and Education Center, University of Tennessee, Jackson 38301; second author: Department of Plant Pathology, University of Florida, Gainesville 32611; third and ninth authors: United States Department of Agriculture–Agricultural Research Service and Department of Crop Sciences, University of Illinois, Urbana 61801; fourth author: Departments of Plant Pathology and Meteorology, Pennsylvania State University, University Park 16802; fifth author: Department of Plant Pathology and Crop Physiology, Louisiana State University Agricultural Center, Baton Rouge 70803; sixth author: Department of Plant Pathology, University of Nebraska-Lincoln, Lincoln 68182; seventh author: Department of Agronomy, North Florida Research and Education Center (NFREC), University of Florida, Quincy 32351; and eighth author: Department of Plant Pathology, NFREC, University of Florida, Quincy 32351 and Gainesville 32611. Accepted for publication 9 March 2015. ABSTRACT Kelly, H. Y., Dufault, N. S., Walker, D. R., Isard, S. A., Schneider, R. W., countries in Asia, Africa, and South America, it was clear that this pathogen Giesler, L. J., Wright, D. L., Marois, J. J., and Hartman, G. L. 2015. From could have a major economic impact on the yield of 30 million ha of select agent to an established pathogen: The response to Phakopsora soybean in the United States. The response by agencies within the United pachyrhizi (soybean rust) in North America. Phytopathology 105:905-916. States Department of Agriculture, industry, soybean check-off boards, and universities was immediate and complex. The impacts of some of these The pathogen causing soybean rust, Phakopsora pachyrhizi, was first activities are detailed in this review. The net result has been that the once described in Japan in 1902. The disease was important in the Eastern dreaded disease, which caused substantial losses in other parts of the world, Hemisphere for many decades before the fungus was reported in Hawaii in is now better understood and effectively managed in the United States. The 1994, which was followed by reports from countries in Africa and South disease continues to be monitored yearly for changes in spatial and America. In 2004, P. pachyrhizi was confirmed in Louisiana, making it the temporal distribution so that soybean growers can continue to benefit by first report in the continental United States. Based on yield losses from knowing where soybean rust is occurring during the growing season. The pathogen causing soybean rust, Phakopsora pachyrhizi Syd., polymerase chain reaction (PCR) primers specific to P. pachyrhizi was first described in Japan in 1902 (Hennings 1903). Over the next 90 identified 11 occurrences of P. pachyrhizi in rust herbarium years, the fungus was reported on soybean and related species specimens, including a 1912 soybean leaf from Japan, a 1913 leaf throughout the Eastern Hemisphere, including Australia, China, India, of Pachyrhizus sp. from Taiwan, and a 1924 leaf of Pueraria sp. Indonesia, Japan, Taiwan, and other countries in tropical and subtropical from the Philippines; P.pachyrhizi was not found outside of Asia or regions (Bromfield 1984). By 1994, P.pachyrhizi had spread beyond the Australia before 1994, indicating that P. pachyrhizi may have been Eastern Hemisphere and into Hawaii (Killgore et al. 1994) and, just endemic to the Eastern Hemisphere (Haudenshield and Hartman a few years later, it was reported in many countries in Africa and South 2015) despite an early report of its occurrence in Africa in the 1970s America. In Africa, P. pachyrhizi was reported in Kenya, Rwanda, (Javid and Ashraf 1978). The potential threat of soybean rust to and Uganda in 1996, followed by Zambia and Zimbabwe in 1998, soybean in the United States was nevertheless recognized, and Nigeria in 1999, Mozambique in 2000, South Africa in 2001, Ghana research on the pathogen began at what is now called the United and the Democratic Republic of Congo in 2007, and Malawi and States Department of Agriculture–Agricultural Research Service Tanzania in 2014 (Murithi et al. 2015). In South America, the first (USDA-ARS) Foreign Disease-Weed Science Research Unit reports of P. pachyrhizi were in Paraguay, followed by Brazil, in (FDWSRU) Biosafety Level 3 (BSL-3) plant pathogen containment 2001 (Yorinori et al. 2005). In 2004, soybean leaf samples from facility at Fort Detrick, MD in 1972 (Bonde and Peterson 1995). a location north of the equator in Columbia tested positive for The emergence of P. pachyrhizi as a major soybean pathogen in P. pachyrhizi (Isard et al. 2005) and, on 6 November 2004, the countries in Africa and South America prompted additional concerns disease was discovered in Louisiana (Schneider et al. 2005). Over and allocation of resources in the United States to address soybean the subsequent decade, P. pachyrhizi was recorded in soybean and rust. On 16 January 2004, the USDA published a detailed and jicama production regions in Mexico, and seasonally on soybean prescient document entitled “National Strategic Plan for the and kudzu in 17 U.S. states, and at a single location on soybean in Integration and Coordination of Soybean Rust Research” (USDA Ontario, Canada (http://sbr.ipmpipe.org). 2004). Preceding this plan, there were several research projects The early movement of P. pachyrhizi in the Eastern Hemisphere headed by U.S. scientists working outside the country that were is not well documented. A recent study using quantitative launched to assess fungicide efficacy, soybean rust resistance, aspects of fungal biology, and disease epidemiology (Isard et al. Corresponding author: G. L. Hartman; E-mail address: [email protected] 2006a; Miles et al. 2003a,b, 2006, 2007). This early work, along with information and warnings from international colleagues about http://dx.doi.org/10.1094/PHYTO-02-15-0054-FI P.pachyrhizi, especially from Brazil and Paraguay, and interactions This article is in the public domain and not copyrightable. It may be freely reprinted with customary crediting of the source. The American Phytopathological Society, with scientists at the USDA-ARS facility in Fort Detrick, where 2015. researchers had worked on the fungus for the past several decades Vol. 105, No. 7, 2015 905 (Bonde and Peterson 1995), provided the knowledge base in the incompatible interaction, branching of fungal hyphae in the United States to have grower meetings and educational workshops mesophyll is not common, and is associated with mesophyll cell to teach others more about soybean rust and P. pachyrhizi.A necrosis (McLean 1979). During the 24 h after inoculation, spore workshop was organized at Fort Detrick in April 2004 in which germination, appressorium formation, and fungal penetration of the participants could view soybean rust firsthand in their secure epidermis in susceptible and resistant soybean genotypes are greenhouses, and this experience was instrumental in being able to similar but, within 2 days, more hyphae occur in the mesophyll recognize the disease in a production field in Louisiana in tissue of susceptible than in resistant genotypes, and mesophyll cell November of that year. These experiences provided pathologists death is greater in soybean genotype with an immune response, in the United States with the tools needed to address soybean rust demonstrating that an incompatible soybean–P.pachyrhizi interaction and to monitor its progress. restricts hyphal development in the mesophyll cell tissue (Vittal et al. 2014).