Abstract
Soybean rust (SBR) caused by Phakopsora pachyrhizi Syd. is one of the most economically important foliar diseases of soybean [Glycine max (L.) Merr.]. At least 52 soybean plant introductions (PIs) with resistance to SBR have a resistance gene at the Rpp3 locus on chromosome 6, but little is known about the degree of similarity between those alleles and the Rpp3 alleles from PI 462312 and ‘Hyuuga’, which has resistance genes at the Rpp3 and Rpp5 loci. Reactions of 52 PIs to a panel of 13 P. pachyrhizi isolates from the United States were assessed to identify accessions with reaction patterns that differed from those of PI 462312 and Hyuuga. Thirty-two PIs were similar to PI 462312 and eight more similar to Hyuuga. Twelve PIs had reactions to 2011 and 2012 isolates from Florida that differed from both PI 462312 and Hyuuga. Although the majority of the 52 accessions appear to have the same Rpp3 allele as PI 462312, at least some of the 12 PIs with different reaction patterns are likely to have unique alleles. This information will be useful in breeding rust-resistant soybean cultivars, and potentially for identifying regions of the Rpp3 locus that are involved in P. pachyrhizi pathotype recognition. None of the P. pachyrhizi isolates collected after 2012 were as virulent as 2011 and 2012 isolates from north-central Florida, demonstrating that virulence shifts in P. pachyrhizi populations are not necessarily permanent.
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Abbreviations
- BSA:
-
Bulked segregant analysis
- Chr:
-
Chromosome
- GRIN:
-
Germplasm Resources Information Network
- IM:
-
Immune (i.e., symptomless) infection type
- MG:
-
Maturity group
- PI:
-
Plant introduction
- RB:
-
Reddish-brown (resistant) infection type
- SBR:
-
Soybean rust
- TAN:
-
Tan (susceptible) infection type
References
Akamatsu H, Yamanaka N, Yamaoka Y, Soares RM, Morel W, Ivancovich AJG, Suenaga K (2013) Pathogenic diversity of soybean rust in Argentina, Brazil, and Paraguay. J Gen Plant Pathol 79:28–40
Akamatsu H, Yamanaka N, Soares RM, Ivanovich AJG, Lavilla MA, Bogado AN, Morel G, Scholz R, Yamaoka Y, Kato M (2017) Pathogenic variation of South American Phakopsora pachyrhizi populations isolated from soybeans from 2010 to 2015. Jpn Agric Res Q 51:221–232. https://www.jircas.go.jp
Bernard RL, Cremeens CR (1988) Registration of ‘Williams 82’ soybean. Crop Sci 28:1027
Boerma HR, Monteros MJ, Ha B-K, Wood ED, Phillips DV, Walker DR, Missaoui AM (2011) Registration of Asian soybean rust-resistant soybean germplasm G01-PR16. J Plant Regist 5:118–122. https://doi.org/10.3198/jpr2009.12.0732crg
Bonde MR, Nester SE, Austin CN, Stone CL, Frederick RD, Hartman GL, Miles MR (2006) Evaluation of virulence of Phakopsora pachyrhizi and P. meibomiae isolates. Plant Dis 90:708–716. https://doi.org/10.1094/PD-90-0708
Bromfield KR (1984) Soybean rust. Monograph no. 11. American Phytopathological Society, St. Paul, MN, USA
Bromfield KR, Hartwig EE (1980) Resistance to soybean rust and mode of inheritance. Crop Sci 20:254–255
Chakraborty N, Curley J, Frederick RD, Hyten DL, Nelson RL, Hartman GL, Diers BW (2009) Mapping and confirmation of a new allele at Rpp1 from soybean PI 594538A conferring RB lesion-type resistance to soybean rust. Crop Sci 49:783–790. https://doi.org/10.2135/cropsci2008.06.0335
Childs SP, Buck JW, Li Z (2018a) Breeding soybeans with resistance to soybean rust (Phakopsora pachyrhizi). Plant Breed 137:250–261. https://doi.org/10.1111/pbr.12595
Childs SP, King ZR, Walker DR, Harris DK, Pedley KF, Buck JW, Boerma HR, Li Z (2018b) Discovery of a seventh Rpp soybean rust resistance locus in soybean accession PI 605823. Theor Appl Genet 131:27–41. https://doi.org/10.1007/s00122-017-2983-4
Diers BW, Kim K-S, Frederick RD, Hartman GL, Unfried J, Schultz S, Cary T (2013) Registration of eight soybean germplasm lines resistant to soybean rust. J Plant Regist 8:96–101. https://doi.org/10.3198/jpr2012.11.0052crg
Galili T (2015) dendextend: an R package for visualizing, adjusting, and compareing tries of hierarchical clustering. Bioinformatics 31:3718–3720. https://doi.org/10.1093/bioinformatics/btv428
Garcia A, Calvo ÉS, Kiihl RAS, Harada A, Hiromoto DM, Vieira LGE (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor Appl Genet 117:545–553. https://doi.org/10.1007/s00122-008-0798-z
Godoy CV, Seixas CDS, Soares RM, Marcelino-Guimaraes FC, Meyer MC, Costamilan LM (2016) Asian soybean rust in Brazil: past, present, and future. Pesqui Agropecu Bras 51:407–421. https://doi.org/10.1590/S0100-204X2016000500002
Harris DK, Kendrick MD, King ZR, Pedley KF, Walker DR, Cregan PB, Buck JW, Phillips DV, Li Z, Boerma HR (2015) Identification of unique genetic sources of soybean rust resistance from the USDA soybean germplasm collection. Crop Sci 55:2161–2176. https://doi.org/10.2135/cropsci2014.09.0671
Hartman GL, Sikora EJ, Rupe JC (2015) Rust. In: Hartman GL, Rupe JC, Sikora EJ, Domier LL, Davis JA, Steffey KL (eds) Compendium of soybean diseases and pests. American Phytopathological Society, St. Paul, MN, USA, pp 56–59
Hartwig EE (1986) Identification of a fourth major gene conferring resistance to soybean rust. Crop Sci 26:1135–1136
Hartwig EE, Bromfield KR (1983) Relationships among three genes conferring specific resistance to rust in soybeans. Crop Sci 23:237–239
Hossain M, Akamatsu MH, Morishita M, Mori T, Yamaoka Y, Suenaga K, Yamanaka N (2014) Molecular mapping of Asian soybean rust resistance in soybean landraces PI 594767A, PI 587905 and PI 416764. Plant Pathol 64:147–156. https://doi.org/10.1111/ppa.12226
Hyten DL, Hartman GL, Nelson RL, Frederick RD, Concibido VC, Narvel JM, Cregan PB (2007) Map location of the Rpp1 locus that confers resistance to soybean rust in soybean. Crop Sci 47:835–838. https://doi.org/10.2135/cropsi2006.07.0484
Hyten DL, Smith JR, Frederick RD, Tucker ML, Song Q, Cregan PB (2009) Bulked segregant analysis using the GoldenGate assay to locate the Rpp3 locus that confers resistance to soybean rust in soybean. Crop Sci 49:265–271. https://doi.org/10.2135/cropsci2008.08.0511
Isard SA, Russo JM, Magarey RO, Golod J, VanKirk JR (2015) Integrated pest information platform for extension and education iPiPE: progress through sharing. J Integr Pest Manag 6:15. https://doi.org/10.1093/jipm/pmv013
Ivancovich A (2005) Soybean rust in Argentina. Plant Dis 89:667–668
Kelly HY, Dufault NS, Walker DR, Isard SA, Schneider RW, Giesler LJ, Wright DL, Marois JJ, Hartman GL (2015) From select agent to an established pathogen: the response to Phakopsora pachyrhizi (soybean rust) in North America. Phytopathology 105:905–916. https://doi.org/10.1094/PHYTO-02-15-0054-FI
Kendrick MD, Harris DK, Ha B, Hyten DL, Cregan PB, Frederick RD, Boerma HR, Pedley KF (2011) Identification of a second Asian soybean rust resistance gene in Hyuuga soybean. Phytopathology 101:535–543
King ZR, Harris DK, Wood ED, Buck JW, Boerma HR, Li Z (2016) Registration of four near-isogenic soybean lines of G00–3213 for resistance to Asian soybean rust. J Plant Regist 10:189–194. https://doi.org/10.3198/jpr2015.04.0027crg
Klosowski AC, May De Mio LL, Miessner S, Rodrigues SG (2015) Detection of the F129L mutation in the cytochrome b gene in Phakopsora pachyrhizi. Pest Manag Sci 72:1211–1215
Kumudini S, Godoy CV, Board JE, Omielan J, Tollenar M (2008) Mechanisms involved in soybean rust-induced yield reduction. Crop Sci 48:2334–2342. https://doi.org/10.2135/cropsci2008.01.0009
Li S, Smith JR, Ray JD, Frederick RD (2012) Identification of a new soybean rust resistance gene in PI 567102B. Theor Appl Genet 125:133–142. https://doi.org/10.1007/s00122-012-1821-y
Mclean RJ, Byth DE (1980) Inheritance of resistance to rust (Phakopsora pachyrhizi) in soybeans. Aust J Agric Res 31:951–956
Miles MR, Frederick RD, Hartman GL (2006) Evaluation of soybean germplasm for resistance to Phakopsora pachyrhizi. Plant Health Prog. https://doi.org/10.1094/php-2006-0104-01-rs
Miles MR, Morel W, Ray JD, Smith JR, Frederick RD, Hartman GL (2008) Adult plant evaluation of soybean accessions for resistance to Phakopsora pachyrhizi in the field and greenhouse in Paraguay. Plant Dis 92:96–105
Miles MR, Bonde MR, Nester SE, Berner DK, Frederick RD, Hartman GL (2011) Characterizing resistance to Phakopsora pachyrhizi in soybean. Plant Dis 95:577–581. https://doi.org/10.1094/PDIS-06-10-0450
Monteros MJ, Missaoui AM, Phillips DV, Walker DR, Boerma HR (2007) Mapping and confirmation of the ‘Hyuuga’ red-brown lesion resistance gene for Asian soybean rust. Crop Sci 47:829–836. https://doi.org/10.2135/cropsci06.07.0462
Paul C, Hartman GL (2009) Sources of soybean rust resistance challenged with single-spored isolates of Phakopsora pachyrhizi. Crop Sci 49:1781–1785
Paul C, Hill CB, Hartman GL (2011) Comparison of visual rust assessments and DNA levels of Phakopsora pachyrhizi in soybean genotypes varying in rust resistance. Plant Dis 95:1007–1012
Paul C, Hartman GL, Marois JJ, Wright DL, Walker DR (2013) First report of Phakopsora pachyrhizi adapting to soybean genotypes with Rpp1 or Rpp6 rust resistance genes in field plots in the USA. Plant Dis 97:1379
Paul C, Frederick RD, Hill CB, Hartman GL, Walker DR (2015) Comparison of pathogenic variation among Phakopsora pachyrhizi isolates collected from the USA and international locations, and identification of soybean genotypes resistant to the USA isolates. Plant Dis 99:1059–1069
Paul C, Motter HZ, Walker DR (2020) Reactions of soybean germplasm accessions to six Phakopsora pachyrhizi isolates from the United States. Plant Dis 104:1087–1095. https://doi.org/10.1049/PDIS-09-18-1704-RE
Pierozzi PHB, Ribeiro AS, Moreira JUV, Laperuta LDC, Rachid BF, Lima WF, Arias CAA, Oliveira MF, Toledo JFF (2008) New soybean (Glycine max Fabales, Fabaceae) sources of qualitative genetic resistance to Asian soybean rust caused by Phakopsora pachyrhizi (Uredinales, Phakopsoraceae). Genet Mol Biol 31:505–511
Ray JD, Morel W, Smith JR, Frederick RD, Miles MR (2009) Genetics and mapping of adult plant rust resistance in soybean PI 587886 and PI 587880A. Theor Appl Genet 119:271–280
Ray JD, Smith JR, Morel W, Bogado AN, Walker DR (2011) Genetic resistance to soybean rust in PI 567099A is at or near the Rpp3 locus. J Crop Improv 25:219–231
Schneider RW, Hollier CA, Whitam HK, Palm ME, McKemy JM, Hernandez JR, Levy L, DeVries-Paterson R (2005) First report of soybean rust caused by Phakopsora pachyrhizi in the continental United States. Plant Dis 89:774
Silva D, Yamanaka N, Brogin R, Arias C, Nepomuceno A, Di Mauro A, Pereira S, Nogueira L, Passianotto A, Abdelnoor R (2008) Molecular mapping of two loci that confer resistance to Asian rust in soybean. Theor Appl Genet 117:57–63
Singh BB, Thapliyal PN (1977) Breeding for resistance to soybean rust in India. In: Ford RE, Sinclair JB (eds) Rust of soybeans: The problem and research needs. Int Agric Pub, INTSOY Ser. No. 12, University of Illinois, Urbana, IL, USA, 62–65
Twizeyimana M, Hartman GL (2012) Pathogenic variation of Phakopsora pachyrhizi isolates on soybean in the USA from 2006 to 2009. Plant Dis 96:75–81
Vuong TD, Walker DR, Nguyen BT, Nguyen TT, Dinh HX, Hyten DL, Nguyen T (2016) Molecular characterization of resistance to soybean rust (Phakopsora pachyrhizi Syd. & Syd.) in soybean cultivar DT 2000 (PI 635999). PLoS ONE 11:e0164493. https://doi.org/10.1371/journal.pone.0164493
Walker DR, Boerma HR, Philips DV, Schneider RW, Buckley JB, Shipe ER, Mueller JD, Weaver DB, Sikora EJ, Moore SH, Hartman GL, Miles MR, Harris DK, Wright DL, Marois JJ, Nelson RL (2011) Evaluation of USDA soybean germplasm accessions for resistance to soybean rust in the southern United States. Crop Sci 51:678–693. https://doi.org/10.2135/cropsci2010.06.0340
Walker DR, Harris DK, King ZR, Li Z, Boerma HR, Buckley JB, Weaver DB, Sikora EJ, Shipe ER, Mueller JD, Buck JW, Schneider RW, Marois JJ, Wright DL, Nelson RL (2014a) Evaluation of soybean germplasm accessions for resistance to Phakopsora pachyrhizi populations in the southeastern United States, 2009–2012. Crop Sci 54:1673–1689. https://doi.org/10.2135/cropsci2013.08.0513
Walker DR, Harris DK, King ZR, Li Z, Phillips DV, Buck JW, Nelson RL, Boerma HR (2014b) Reactions of soybean germplasm accession seedlings to soybean rust (Phakopsora pachyrhizi) isolates from Georgia. Crop Sci 54:1433–1447. https://doi.org/10.2135/cropsci2013.09.0654
Ward JH Jr (1963) Hierarchical grouping to optimize and objective function. J Am Stat Assoc 58:236–244
Wrather JA, Koenning SR (2009) Effects of diseases on soybean yields in the United States 1996 to 2007. Plant Health Prog. https://doi.org/10.1094/PHP-2009-0401-01-RS
Wrather JA, Shannon G, Balardin R, Carregal L, Escobar R, Gupta GK, Ma Z, Morel W, Ploper D, Tenuta A (2010) Effect of diseases on soybean yield in the top eight producing countries in 2006. Plant Health Progress. https://doi.org/10.1094/PHP-2010-0125-01-RS
Yamanaka N, Hossain MN (2019) Pyramiding three rust-resistance genes confers a high level of resistance in soybean (Glycine max). Plant Breed 138:686–695
Yamanaka N, Yamaoka Y, Kato M, Lemos N, Passianotto AL, Santos JVM, Benitez ER, Abdelnoor RV, Soares RM, Suenaga K (2010) Development of classification criteria for resistance to soybean rust and differences in virulence among Japanese and Brazilian rust populations. Trop Plant Pathol 35:153–162
Yamanaka N, Lemos NG, Uno M, Akamatsu H, Yamaoka Y, Abdelnoor RV, Braccini ALE, Suenaga K (2013) Resistance to Asian soybean rust in soybean lines with the pyramided three Rpp genes. Crop Breed Appl Biotechnol 13:75–82
Yang XB, Tschanz AT, Dowler WM, Wang TC (1991) Development of yield loss models in relation to reduction of components of soybean infected with Phakopsora pachyrhizi. Phytopathology 81:1420–1426
Yorinori JT, Paiva WM, Frederick RD, Costamilan LM, Bertagnolli PF, Hartman GL, Godoy CV, Nunes J Jr (2005) Epidemics of soybean rust (Phakopsora pachyrhizi) in Brazil and Paraguay from 2001–2003. Plant Dis 89:675–677. https://doi.org/10.1094/PD-89-0675
Yu N, Kim M, King ZR, Harris DK, Buck JW, Li Z, Diers BW (2015) Fine mapping of the Asian soybean rust resistance gene Rpp2 from soybean PI 230970. Theor Appl Genet 128:387–396. https://doi.org/10.1007/s00122-014-2438-0
Acknowledgements
We are grateful to the USDA Agricultural Research Service and to the United Soybean Board for partial financial support of this research (Project no. 3611-22000-019-30R). We thank the donors of P. pachyrhizi samples, including Jim Marois and G. Kelly O’Brien (North Florida Res. & Ed. Center), Clayton Hollier (Louisiana State University); Ed Sikora (Auburn University, Alabama); and Glen Hartman (USDA-ARS, Urbana, IL). We also thank Wei Wei, Leticia Lamana, Heather Lash, and Andrew D’Urso at the University of Illinois and Randy Nelson (retired) and Todd Bedford of the USDA Soybean Germplasm Collection in Urbana, IL, USA.
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Paul, C., Harris, D.K., Li, Z. et al. Reactions of 52 soybean germplasm accessions with Rpp3 alleles to a panel of 13 Phakopsora pachyrhizi (soybean rust) isolates from the southern United States. J Gen Plant Pathol 87, 55–70 (2021). https://doi.org/10.1007/s10327-020-00972-w
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DOI: https://doi.org/10.1007/s10327-020-00972-w