Forty years ago, the US Department of Agriculture (USDA) Forest Service developed and currently operates the Resistance Screening Center near Asheville, North Carolina, as a service to both industry and university-based tree improvement programs and tree-seed exporting companies in the southern US, Mexico, and Central America. Seed lots from more than 15,000 selections of slash and loblolly pines have been evaluated for genetically-controlled resistance to fusiform rust and other diseases including pitch canker, dogwood anthracnose, and brown spot needle blight. The screening system uses a greenhouse-based artificial inoculation system with controlled density of inoculum from geographically diverse sources of the rust pathogen. Results are completed in 6–9 months and are reasonably well-correlated with field-based progeny tests. Operating costs of the Center are shared by both the USDA Forest Service and its clients. The technologically sophisticated methods and professional skills of the Center staff have been applied to facilitate and accelerate progress in region-wide timber production, scientific understanding of the fusiform rust pathosystem, and graduate education of forest geneticists and pathologists in universities.
References
[1]
Hodges, C.S., Jr. Diseases in Southeastern Forest Nurseries and Their Control. Research Paper 142; U.S. Department of Agriculture Forest Service, Southeast Forestry Experiment Station: Asheville, NC, USA, 1962; p. 16.
[2]
Siggers, P.V.; Lindgren, R.M. An old disease—A new problem. South. Lumberm. 1947, 175, 172–175.
[3]
Miller, T. Influence of site preparation and spacing on the incidence of fusiform rust in planted slash pines. For. Sci. 1970, 18, 70–75.
[4]
Boggess, W.R.; Stahelin, R. The incidence of fusiform rust in slash pine plantations receiving cultural treatments. J. For. 1948, 46, 683–685.
[5]
Powers, H.R. Reductions of disease losses in pine plantations. ALA For. Prod. 1969, 12, 71–75.
[6]
Jewell, F.F. Disease Resistance Studies in Tree Improvement Research. In Proceeding of the Fifth Southern Conference on Forest Tree Improvement, Raleigh, NC, USA, 11–12 June 1959; pp. 18–20.
[7]
Jewell, F.F. Infection of artificially inoculated shortleaf pine hybrids with fusiform rust. Plant Dis. Reptr. 1961, 45, 639–640.
[8]
Barber, J.C. Inherent Variation among Slash Pine Progenies at the Ida Cason Callaway Foundation. Research Paper SE-10; Department of Agriculture Forest Service, Southeast Forestry Experiment Station: Asheville, NC, USA, 1964; p. 90.
[9]
Jewell, F.F.; Henry, B.W. Breeding for resistance to southern fusiform rust. Proc. Ninth Intern. Congr. 1966, 2, 1694–1695.
[10]
Kinloch, B.B.; Stonechpher, R.W. Genetic variation in susceptibility to fusiform rust in seedlings from a wild population of loblolly pine. Phytopathology 1969, 59, 1246–1255.
[11]
Blair, R.L. Quantitative Inheritance of Resistance to Fusiform Rust in Loblolly Pine. Ph.D. Thesis, North Carolina State University, Raleigh, NC, USA, 1970.
[12]
Wells, O.O.; Wakeley, P.C. Geographic variation in survival, growth, and fusiform rust infection in planted loblolly pine. For. Sci. Monogr. 1966, 11, 40.
[13]
Jewell, F.F.; Mallet, S.L. Resistance to fusiform rust in slash pine as shown by artificial inoculation. Phytopathology 1964, 54, 1294.
[14]
Goddard, R.E.; Arnold, J.T. Screening Select Slash Pines for Resistance to Fusiform Rust by Artificial Inoculation. In Breeding Pest-Resistant Trees; Gerhold, H.D., Schreiner, E.J., McDermott, R.E., Winieski, W.A., Eds.; Pergamon Press: New York, NY, USA, 1966; pp. 431–435.
[15]
Snow, G.A. Time required for infection of pine by Cronartium. fusiforme and effect of field and laboratory exposure after inoculation. Phytopathology 1968, 15, 1547–1550.
[16]
Schmidt, R.A. A Literature Review of Inoculation Techniques Used in Studies of Fusiform Rust. In Biology of Rust Resistance in Forest Trees, Proceedings of a NATO-IUFRO Advanced Study Institute, Moscow, ID, USA, 17–24 August 1969; pp. 341–356.
[17]
Dinus, R.J. Testing slash pine for rust resistance in artificial and natural conditions. In Proceedings of the 10th Southern Forest Tree Improvement Conference, Houston, TX, USA, 17–19 June 1969; pp. 98–106.
[18]
Dwinell, L.D. An inoculation system for Cronartium. fusiforme. In Biology of Rust Resistance in Forest Trees, Proceedings of a NATO-IUFRO Advanced Study Institute, Moscow, ID, USA, 17–24 August 1969; pp. 327–330.
[19]
Miller, T. Inoculation of slash pine seedlings with stored basidiospores of Cronartium fusiforme. Phytopathology 1970, 60, 1773–1774, doi:10.1094/Phyto-60-1773.
[20]
Von Weissenberg, K.; Lewis, R.A.; Cowling, E.B. Fusiform Rust Aeciospore Bank. In Proceedings of the Southwide Forest Disease Conference, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA, 8–10 June 1971; p. 1.
[21]
Matthews, F.R.; Rowan, S.J.; Dwinell, L.D.; Duncan, H.J. Procedures Used in Fusiform Rust Research. Office Report; Southeastern Forest Experiment Station: Athens, GA, USA, 1971; p. 16.
[22]
Knighten, J.L.; Young, C.H.; McCartney, T.C.; Anderson, R.A. Resistance Screening Center Procedures Manual: A Step-by-Step Guide Used in the Operational Screening of Southern Pines for Resistance to Fusiform Rust; USDA Forest Service: Asheville, NC, USA, 1988; p. 62.
[23]
Young, C.H.; Minton, B.S.; Bronson, J.J. Resistance Screening Center Procedures Manual: A Step-by-Step Guide Used in the Operational Screening of Southern Pines for Resistance to Fusiform Rust; USDA Forest Service: Asheville, NC, USA, 2006; p. 52.
[24]
Laird, P.P.; Knighten, J.L.; Wolfe, R.L. Basic Methodology Used at the Fusiform Rust Testing Facility; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1973; p. 14.
[25]
Laird, P.P.; Knighten, J.L.; Wolfe, R.L. An Evaluation of a Method for Use in Determining Relative Rust Resistance in Loblolly and Slash Pine Families. Forest Tree Resistance Testing Facility Report Number 1; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1974; p. 48.
[26]
Anderson, R.L.; Powers, H.R. The Resistance Screening Center—Screening for Disease Resistance as a Service for Tree Improvement Programs. In Proceedings of the Rusts of Hard Pines Working Party Conference (S2.06–10), Athens, GA, USA, 31 July–6 August 1983; Barrows-Broaddus, J., Powers, H.R., Eds.; pp. 59–65.
[27]
Triplett, J.D. Evaluation of a New Seedling Container Design at the Resistance Screening Center; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1982; p. 8.
[28]
Anderson, R.L.; Hubbard, S.D.; Ryan, G.W. Comparison of Two Pine Seedling Container Systems Used at the Resistance Screening Center. In Tree Planter’s Notes Summer; USDA: Washington, DC, USA, 1982; pp. 27–30.
[29]
Laird, P.P.; Knighten, J.L.; Wolfe, R.L. Reduced Inoculum Density Enhances Sensitivity of Resistance Screening Detection in Fusiform Rust Resistance Testing. Report Number 74-1-10; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1974; p. 10.
[30]
Hubbard, S.D. Resistance Screening Center Test 103–80. Report No. 80-1-24; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1980; p. 8.
[31]
Hubbard, S.D.; Triplett, J.D.; Oak, S. Inoculation Systems Comparison at the Resistance Screening Center. Report No. 81-1-39; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1981; p. 6.
[32]
Gramacho, K.P.; Miller, T.; Schmidt, R.A. Comparative histopathology of host reaction types in slash pine resistant to Cronartium. quercum f.sp. fusiforme. Forests 2013, 4, 319–328, doi:10.3390/f4020319.
[33]
Nelson, C.D.; Kubisiak, T.L.; Amerson, H.V. Unraveling and managing fusiform rust disease: A model approach for coevolved forest tree pathosystems. For. Path. 2010, 40, 67–72.
[34]
Isik, F.; Amerson, H.V.; Whetten, R.S.; Garcia, S.A.; McKeand, S.E. Interactions of Fr genes and mixed-pathogen inocula in the loblolly pine-fusiform rust pathosystem. Tree Genet. Genomes 2012, 8, 15–25, doi:10.1007/s11295-011-0416-0.
[35]
Kubisiak, T.L.; Anderson, C.L.; Amerson, H.V.; Smith, J.A.; Davis, J.M.; Nelson, C.D. A genomic map enriched for markers linked to Avr1 in Cronartium. quercuum f.sp. fusiforme. Fungal Genet. Biol. 2011, 48, 266–274, doi:10.1016/j.fgb.2010.09.008.
[36]
Schmidt, R.A.; Gramacho, K.P.; Miller, T.; Young, C.H. Components of partial resistance in the slash pine-fusiform rust pathosystem. Phytopathology 2000, 90, 1005–1010, doi:10.1094/PHYTO.2000.90.9.1005.
[37]
Gramacho, K.P.; Schmidt, R.A.; Miller, T. Stability of slash pine families with major gene and partial resistance to single gall and mixed gall inocula of Cronartium quercum f. sp. fusiforme in greenhouse studies. Forests 2013, 4, 488–499, doi:10.3390/f4020488.
[38]
Hubbard, S.D. An Index for Selection of Relative Rust Resistance Using Tree Seedling Symptom Types. A Proposition for Partial Fulfillment of Degree Requirements for the Ph.D. at North Carolina State University, Raleigh, NC, USA, 1981, 25.
[39]
Walkinshaw, C.H.; Hubbard, S.D.; Triplett, J.; Anderson, R.L. How to Identify Six Different Fusiform Rust Symptom Types on Seedlings at the Resistance Screening Center. Report No. 82-1-5; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1981; p. 8.
[40]
Walkinshaw, C.H.; Dell, T.R.; Hubbard, S.D. Predicting Field Performance of Slash Pine Families from Inoculated Greenhouse Seedlings. Research Paper SO-160; USDA Forest Service: Gulfport, MS, USA, 1980; p. 6.
[41]
Hatcher, A. A Comparison of Rust Resistance Evaluations: Field Tests vs. Resistance Screening Center Tests; N.C. State University-Industry Cooperative Tree Improvement Cooperative, NC State University: Raleigh, NC, USA, 1992; p. 10.
[42]
Hatcher, A. A Comparison of Rust Resistance Evaluations: Field Tests vs. Resistance Screening Center Tests; N.C. State University-Industry Cooperative Tree Improvement Cooperative, NC State University: Raleigh, NC, USA, 1993; p. 30.
[43]
Hatcher, A. A Comparison of Rust Resistance Evaluations: Field Tests vs. Resistance Screening Center Tests; N.C. State University-Industry Cooperative Tree Improvement Cooperative, NC State University: Raleigh, NC, USA, 1995; p. 27.
[44]
Anderson, R.L. New method for assessing contamination of slash and loblolly pine seeds by Fusarium moniliforme var. subglutinans. Plant Dis. 1986, 70, 452–453, doi:10.1094/PD-70-452.
[45]
Anderson, R.L. Pine—Pitch Canker FungusWorksheet No. 56, Chapter 7. In ISTA Handbook on Seed Health Testing; International Seed Testing Association: Zurich, Switzerland, 1987; p. 6.
[46]
Blakeslee, G.; Oak, S.W. Pitch Canker Resistant Slash Pine Identified by Greenhouse Screening at the Resistance Screening Center. Report No. 88-1-44; Forest Pest Management, Field Office: Asheville, NC, USA, 1988; p. 12.
[47]
Young, C.H.; Minton, B.S.; Bronson, J.J. Resistance Screening Center Procedures Manual: A Guide Used in the Operational Screening of Pines for Resistance to Pitch Canker Disease; USDA Forest Service, Forest Health Protection: Asheville, NC, USA, 2006; p. 21.
[48]
Anderson, R.L. Development of an Inoculation System for Infection of Flowering Dogwood with Discula sp. at the Resistance Screening Center. Report No. 91-1-34; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1991; p. 5.
Drummond, D.B. The Feasibility of Screening Southern Pines against Air Pollutants at the Resistance Screening Center; Forest Pest Management, Asheville Field Office: Asheville, NC, USA, 1982; p. 13.
[51]
North Carolina State University Cooperative Tree Improvement Program (NCSUCTIP). Clonal Testing of Atlantic Coastal Elite (ACE) Population. 52nd Annual Report of the North Carolina State University Cooperative Tree Improvement Program; NC State University: Raleigh, NC, USA, 2008; pp. 1–2.
[52]
North Carolina State University Cooperative Tree Improvement Program (NCSUCTIP). Third-Cycle Elite Breeding Progress: Atlantic Coastal Elite (ACE) Population and Elite Diallel Population (PEDP). 56th Annual Report of the North Carolina State University Cooperative Tree Improvement Program; NC State University: Raleigh, NC, USA, 2012; pp. 4–5.
[53]
Nel, A.; Hodge, G.R.; Mongwaketsi, K.E.; Kanzler, A. Variation in pitch canker fungus (Fusarium. circinatum) resistance among open-pollinated families of Pinus. patula tested at screening facilities in the USA and South Africa. South. For. 2013. Submitted.
[54]
Dvorak, W.S.; Hodge, G.R.; Kietzka, J.E. Genetic variation in survival, growth, and stem form of Pinus. leiophylla in Brazil and South Africa and provenance resistance to pitch canker. South. Hemisph. For. J. 2007, 69, 125–135, doi:10.2989/SHFJ.2007.69.3.1.351.
[55]
Dvorak, W.S.; Potter, K.M.; Hipkins, V.D.; Hodge, G.R. Genetic diversity and gene exchange in Pinus. oocarpa, a Mesoamerican pine with resistance to the pitch canker fungus (Fusarium. circinatum). Int. J. Plant Sci. 2009, 170, 609–626.
[56]
Windham, M.T.; Graham, E.T; Witte, E.T.; Knighten, J.L.; Trigiano, R.N. Cornus. florida “Appalachian Spring”: A white flowering dogwood resistant to dogwood anthracnose. Hort. Sci. 1998, 33, 1265–1267.
[57]
Wilcox, P.L.; Amerson, H.V.; Kuhlman, E.G.; Liu, B.H.; O’Malley, D.M.; Sederoff, R.R. Detection of a major gene for resistance to fusiform rust disease in loblolly pine by genomic mapping. Proc. Natl. Acad. Sci. USA 1996, 93, 3859–3864.
[58]
Nelson, C.D.; Doudrick, R.L.; Nance, W.L.; Hamaker, J.M.; Capo, B. Specificity of Host:Pathogen Genetic Interaction for Fusiform Rust Disease on Slash Pine. In Proceeding of the 22nd Southern Forest Tree Improvement Conference, Atlanta, GA, USA, 14—17 June 1993; pp. 403–410.
[59]
Isik, F.; Amerson, H.V.; Whetton, R.W.; Garcia, S.A.; Li, B.; McKeand, S. Resistance of Pinus. taeda families under artificial inoculations with diverse fusiform rust pathogen populations and comparisons with field trials. Can. J. For. Res. 2008, 38, 2687–2696, doi:10.1139/X08-111.
[60]
Kong, X. RAPD Mapping and Its Application in Slash Pine Breeding. Ph.D. Thesis, Texas A&M University, College Station, TX, USA, 1996.
[61]
McKeand, S.; Mullin, T.; Byram, T.; White, T. Deployment of genetically improved loblolly and slash pine in the South. J. For. 2003, 101, 32–37.
[62]
Schmidt, R.A. Fusiform Rust Disease of Southern Pines: Biology, Ecology and Management. Technical Bulletin 903; University of Florida, Agricultural Experiment Station, Institute of Food and Agricultural Sciences: Gainesville, FL, USA, 1998; p. 14.
[63]
Schmidt, R.A. Fusiform rust of southern pines: A major success for forest disease management. Phytopathology 2003, 93, 1048–1051, doi:10.1094/PHYTO.2003.93.8.1048.
[64]
Dinus, R.J.; Schmidt, R.A. Management of fusiform rust in southern pines. In Proceedings of a Symposium Sponsored by the Southern Forest Disease and Insect Research Council, University of Florida, Gainesville, FL, USA, 7–8 December 1976.
[65]
Cubbage, F.W.; Pye, J.M.; Holmes, T.P.; Wagner, J.E. An economic evaluation of fusiform rust research. South. J. Appl. For. 2000, 24, 77–85.
[66]
Starkey, T.E.; Enebak, S.A. The Use of Proline (Prothioconazole) to Control Pitch Canker, Rhizoctonia Foliage Blight, and Fusiform Rust in Forest Seedling Nurseries and Efforts to Acquire Registration. In National Proceedings: Forest and Conservation Nursery Associations—2010. Proc. RMRS-P-65; Riley, L.E., Haase, D.L., Pinto, J.R., Eds.; USDA Forest Service, Rocky Mountain Research Station: Fort Collins, CO, USA, 2011; pp. 49–57.
[67]
Enebak, S.A. New Fungicide to Treat Pine Seedling Diseases. Alabama’s TREASURED Forests Magazine—Fall 2012; Alabama Forestry Commission: Montgomery, AL, USA, 2012; p. 30.
