Introduction of Asian Soybean Rust Urediniospores Into the Midwestern United States—A Case Study
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Introduction of Asian Soybean Rust Urediniospores into the Midwestern United States—A Case Study Sagar Krupa, Department of Plant Pathology, University of Minnesota, St. Paul 55108; Van Bowersox and Roger Claybrooke, Illinois State Water Survey, National Atmospheric Deposition Program & National Trends Network (NADP & NTN) Programs, Champaign, IL 61820; Charles W. Barnes and Les Szabo, United States Department of Agriculture–Agricultural Research Service, Cereal Disease Laboratory, St. Paul, MN 55108; Karen Harlin, Illinois State Water Survey, NADP & NTN Programs, Champaign; and James Kurle, Department of Plant Pathology, Uni- versity of Minnesota, St. Paul size) that obey the laws of gravity or rapid ABSTRACT sedimentation or settling to the surface Krupa, S., Bowersox, V., Claybrooke, R., Barnes, C. W., Szabo, L., Harlin, K., and Kurle, J. once released into the atmosphere. Thus, 2006. Introduction of Asian soybean rust urediniospores into the midwestern United States—a they cannot travel long distances close to case study. Plant Dis. 90:1254-1259. the surface, within the mixed boundary layer (MBL; the atmosphere influenced by In 2005, weekly rain samples collected at 124 National Atmospheric Deposition Pro- surface heat exchange and turbulent mix- gram/National Trends Network (NADP/NTN) sites in the eastern and central United States were ing). On the other hand, they can travel screened for Asian soybean rust (ASR; Phakopsora pachyrhizi) urediniospores. Application of a long distances once transported upward quantitative polymerase chain reaction method detected P. pachyrhizi DNA in the filter residue of rain samples collected during the week of 19 to 26 July 2005 in Minnesota, Missouri, and above the variable MBL height into the South Dakota. To determine the geographic origin of ASR urediniospores in those weekly com- free troposphere (FT), where there is posite samples, back air trajectories of the lifted condensation and mixed boundary layers were minimal resistance for horizontal transport. calculated for each rain event within the week, by sampling site. The calculations, based on the Once in the FT at large distances from the hybrid single-particle lagrangian integrated trajectory model, pointed to source areas in eastern initial source regions, rain is a major and southern Texas. In a separate case, DNA of P. pachyrhizi was detected in a 28 June to 5 July mechanism for depositing coarse particles, 2005 rain sample from an eastern Texas site. Back trajectories pointed to southern Texas and the including fungal spores, onto the surface Yucatan Peninsula in Mexico as potential source areas of ASR urediniospores. Vertical motions (23). For example, Krupa et al. (13) and of those back trajectories indicated a ventilation of the boundary layer in the upwind areas, sug- Krupa and Nosal (14) showed the impor- gesting the possible injection of urediniospores into the free troposphere where they can be tance of summertime anticyclonic or transported for long distances before wet deposition. clockwise motion of air parcels preceding the wet deposition (precipitation) of high Additional keywords: spore transport concentrations of air pollutants (e.g., par- ticulate sulfate and nitrate) by long-range transport across the central plains into For the first time, Asian soybean rust iniospores from infected plants. ASR is Minnesota. (ASR) disease caused by Phakopsora most likely to survive typical winters in the Although the details of the specific pachyrhizi Sydow was reported in the con- continental United States by persisting on methodologies used for the identification tinental United States during 2004 (30). annual and perennial alternative hosts in of ASR urediniospores will be reported Similar observations also were made in southernmost Texas and Florida, coastal elsewhere, the main objective of the pre- 2005. P. pachyrhizi is an obligate fungal areas of the Gulf States, and southern Cali- sent case study was to examine the poten- parasite that produces both uredinia and fornia. P. pachyrhizi has a wide host range tial for the atmospheric transport of soy- telia in controlled environments, under in the legume family that includes soy- bean rust urediniospores across the central proper conditions (15). However, the alter- bean, dry and snap bean, pea, and a num- plains into the Midwest and for its spread nate host (aecial) is unknown and, there- ber of forage crops (e.g., sweet clover) and from the southern to the northern United fore, little is known about the role of the weeds (e.g., kudzu) (24). Thus, south to States through wet deposition. telial stage in the life cycle of the fungus in north aerial dispersal of urediniospores nature and the rust is thought to rely exclu- from infected hosts will determine whether MATERIALS AND METHODS sively on continuous production of uredin- the rust can occur in the principal soybean- Rain sample collection and sample iospores on a living host for its survival growing areas of the north-central United preparation. At some 124 sites in the (25). Spore dispersal and disease spread is States. Source regions of the fungal inocu- eastern and central United States, weekly, a function of aerial dissemination of ured- lum will be at large distances from the composite rain samples were collected major soybean-growing areas of the upper according to the NADP/NTN (National Midwest; therefore, long-range transport Atmospheric Deposition Program/National Corresponding author: J. Kurle and deposition of viable urediniospores Trends Network) protocol for precipitation E-mail: [email protected] will be an important mechanism for annual sampling (4). The times of occurrence reintroduction of ASR. Experience with (dates and hours) and depths of individual Any findings or conclusions stated in this publica- tion do not necessarily reflect the views of the disease incidence surveys for the rusts of rain events contributing to the weekly United States Department of Agriculture or other corn and small grains indicates that uredin- composite samples were obtained inde- sponsors. iospores from infected plants in Mexico, pendently using chart data from recording, southern Texas, and Louisiana routinely co-located rain gages. After measuring the Accepted for publication 10 April 2006. contribute to development of epidemics in pH and electrical conductance of the rain the north-central United States (28,29). samples in the laboratory for atmospheric DOI: 10.1094/PD-90-1254 Soybean rust urediniospores are coarse deposition and climate-related studies, © 2006 The American Phytopathological Society particles (about 18 to 34 by 15 to 24 µm in they were vacuum filtered. The filters were 1254 Plant Disease / Vol. 90 No. 9 desiccated in clean air and subsequently performed for individual events, with such (TX56; latitude: 33.3917 N, longitude: analyzed for the presence of P. pachyrhizi information derived from the recording 97.6397 W) during 28 June to 5 July 2005 DNA. rain gage co-located with the rain sampler. tested positive for the presence of ASR Identification of soybean rust uredin- Sample from the LBJ Grasslands site. urediniospores (DNA). This sample con- iospores. Rain sample filter residues were Filter residue of the weekly rain sample tained rainfall from two events: (i) 0.05 extracted for DNA and analyzed through collected at the LBJ Grasslands site cm, 1200 to 1300 Zulu Time (i.e., 12Z to the application of a nested quantitative polymerase chain reaction (qPCR; modi- a fied from the PCR procedure of Frederick Table 1. Summary data on rain sample collection and identification of soybean rust DNA et al.; 8) assay using a P. pachyrhizi- NADP Rain sampling Gel DNA specific Taqman probe (C. W. Barnes and site IDb Site name, state period qPCRc electrophoresis sequence L. Szabo, United States Department of TX56 LBJ Grasslands, Texas 28 June to 5 July + + Nd Agriculture–Agricultural Research Ser- MO03 Ashland Wildlife, Missouri 19 July to 26 July + + Nd vice, Cereal Disease Laboratory, St. Paul, SD08 Cottonwood, South Dakota 19 July to 26 July + + Nd MN, unpublished data). Where appropri- MN27 Lamberton, Minnesota 19 July to 26 July + + + ate, the qPCR results were confirmed by a Analysis was performed on composite rain samples collected during the week; + = positive result and gel electrophoresis for the presence of Nd = not done. DNA amplification product corresponding b NADP = National Atmospheric Deposition Program sites (19). to the predicted size for P. pachyrhizi. In c qPCR = quantitative polymerase chain reaction. addition, DNA sequence analysis of se- lected samples was used to further confirm the specificity of the qPCR assay (C. W. Barnes and L. Szabo, unpublished data). Application of an atmospheric parti- cle or spore transport model. For the rain sampling sites and dates listed in Table 1, back air trajectory analyses were performed using the hybrid single-particle lagrangian integrated trajectory (HYSPLIT) model (6) to identify potential ASR source areas and spore transport pathways. The HYSPLIT model was initialized using meteorological data from the National Weather Service’s Eta model. The domain of these data sets the domain limits of HYSPLIT trajectories (21). For each rain event, trajectories were initiated at two heights above the surface and calculated for up to 168 h prior to the event. Those heights were the MBL and the lifting condensation layer (LCL) or the cloud layer at the time of the rain event. The MBL and LCL heights were deter- mined from analysis of National Weather Service atmospheric soundings nearest in time and space to each rain event recorded at the NADP/NTN site. The HYSPLIT model computes the location and height of back trajectories. Vertical wind displace- ments were used to identify areas of possi- ble injection of rust urediniospores into the FT, where the urediniospores could be transported long distances before deposi- tion. Identifying these injection points required determination of the MBL heights from atmospheric soundings along the backward (i.e., upwind) trajectory path- ways. Urediniospores may enter the FT when the trajectory rises from beneath the MBL height into the FT.