Abstract
Asian soybean rust (ASR), caused by the fungus Phakopsora pachyrhizi, is the main disease affecting soybean in Brazil. This study aimed at investigating and mapping the resistance of the PI 594756 to P. pachyrhizi, by using Bulked Segregant Analysis (BSA). The PI 594756 and the susceptible PI 594891 were crossed and the resulting F2 and F2:3 populations (208 and 1770 plants, respectively) were tested against ASR. Also, these PIs and differential varieties were tested against a panel of monosporic isolates. Plants presenting tan lesions were classified as susceptible (S) while plants presenting reddish-brown (RB) lesions were classified as resistant. DNA bulks were genotyped with Infinium BeadChips and the genomic region identified was further analyzed in the F2 individuals with target GBS (tGBS). PI 594,56 presented a unique resistance profile compared to the differential varieties. The resistance was monogenic dominant; however, it was classified as incompletely dominant when quantitatively studied. Genetic and QTL mapping placed the PI 594756 gene between the genomic region located at 55,863,741 and 56,123,516 bp of chromosome 18. This position is slightly upstream mapping positions of Rpp1 (PI 200492) and Rpp1-b (PI 594538A). Finally, we performed a haplotype analysis in a whole genomic sequencing-SNP database composed of Brazilian historical germplasm and sources of Rpp genes. We found SNPs that successfully differentiated the new PI 594756 allele from Rpp1 and Rpp1-b sources. The haplotype identified can be used as a tool for marker-assisted selection (MAS).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All phenotypic and genotypic data is provided in the supplementary material. Re-sequencing data is part of a Genome Wide Association Study still not published. Nonetheless, it can be partially available through direct contact to the corresponding author Dra. Francismar C. Marcelino-Guimarães by email: francismar.marcelino@embrapa.br.
Code availability
Codes used in the study are available in the corresponding references and also through direct contact to the corresponding author Dra. Francismar C. Marcelino-Guimarães by email: francismar.marcelino@embrapa.br.
References
Akamatsu H, Yamanaka N, Yamaoka Y, Soares RM, Morel W, Ivancovich AJG, Bogado AN, Kato M, Yorinori JT, Suenaga K (2013) Pathogenic diversity of soybean rust in Argentina, Brazil, and Paraguay. J Gen Plant Pathol 79:28–40. https://doi.org/10.1007/s10327-012-0421-7
Alonso-Blanco C, Koornneef M, van Ooijen JW (2006) QTL Analysis. In: Salinas J, Sanchez-Serrano JJ (eds) Arabidopsis Protocols. Methods in Molecular Biology™, vol 323. Humana Press. https://doi.org/10.1385/1-59745-003-0:79
Aoyagi LN (2018) Variabilidade Alélica do loci de Rpp1 em Diversos Germoplasmas de soja Caracterizada por GBS e Resequenciamento. Universidade Estadual de Maringá, Thesis
Aoyagi LN, Yukie M, Naoki Y (2020) Characterization of three soybean landraces resistant to Asian soybean rust disease. Mol Breed 40:53. https://doi.org/10.1007/s11032-020-01132-w
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Bromfield KR (1984) Soybean rust. Soybean rust. St. Paul: American Phytopathological Society, p 65. (Monography, 11)
Bromfield KR, Hartwig EE (1980) Resistance to soybean rust and mode of inheritance. Crop Sci 20:254–255
Browning S, Browning B (2007) Rapid and accurate haplotype phasing and missing-data inference for whole genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084–1097
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
Chen H, Zhao S, Yang Z, Sha A, Wan Q, Zhang C, Chen L, Yuan S, Qiu D, Chen S (2015) Genetic analysis and molecular mapping of resistance gene to Phakopsora pachyrhizi in soybean germplasm SX6907. Theor Appl Genet 128:733–743. https://doi.org/10.1007/s00122-015-2468-2
Childs SP, Buck JW, Li Z (2018) 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 (2018) 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
Cook DE, Bayless AM, Wang K, Guo X, Song Q, Jiang J, Bent AF (2014) Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiol 165:630–647. https://doi.org/10.1104/pp.114.235952
Darben LM, Yokoyama A, Castanho FM, Lopes-Caitar VS, Godoy CV, de Carvalho S, Gonela A, Marcelino-Guimarães FC (2020) Characterization of genetic diversity and pathogenicity of Phakopsora pachyrhizi mono-uredinial isolates collected in Brazil. Eur J Plant Pathol 156:355–372. https://doi.org/10.1007/s10658-019-01872-2
Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JD (1998) The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10(11):1915–1925. https://doi.org/10.1105/tpc.10.11.1915
Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931. https://doi.org/10.2135/cropsci1971.0011183X001100060051
Fundação Pró-Sementes: Desempenho de cultivares de soja indicadas para o Rio Grande do Sul. https://fundacaoprosementes.com.br/wp-content/themes/alpina-theme/assets/arq/ECR-SOJA-RS-2012-2013.pdf. Acessed 20 December 2022
Garcia A, Calvo ÉS, de Souza Kiihl RA, Harada A, Hiromoto DM, Vieira LGE (2008) Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor App Genet 117:545–553. https://doi.org/10.1007/s00122-008-0798-z
Garcia A, Calvo ÉS, de Souza Kiihl RA, de Souto ER (2011) Evidence of a susceptible allele inverting the dominance of rust resistance in soybean. Crop Sci 51:32–40. https://doi.org/10.2135/cropsci2010.01.0037
Gebremedhn HM, Msiska UM, Weldekidan MB, Asmamaw FA, Winnifred A, Onziga DI, Odong TL, Rubaihayo P, Tukamuhabwa P (2018) Identification and mapping of quantitative trait loci associated with soybean rust (Phakopsora pachyrhizi) resistance in genotype UG 5. Afr J Biotechnol 17:1368–1376. https://doi.org/10.5897/AJB2018.16661
Gebremedhn HM, Msiska UM, Weldekidan MB, Odong TL, Rubaihayo P, Tukamuhabwa P (2020) Prediction of candidate genes associated with resistance to soybean rust (Phakopsora pachyrhizi) in line UG-5. Plant Breed 00:1–7. https://doi.org/10.1111/pbr.12847
Godoy CV, Seixas CDS, Soares RM, Marcelino-Guimarães FC, Meyer MC, Costamilan LM (2016) Asian soybean rust in Brazil: past, present, and future. Pesq Agrop Brasileira 51:407–421. https://doi.org/10.1590/S0100-204X2016000500002
Hammond-Kosack KE, Jones JD (1994) Incomplete dominance of tomato Cf genes for resistance to Cladosporium fulvum. Mol Plant Microbe Interact 7:58–58. https://doi.org/10.1094/MPMI-7-0058
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
Hossain MM, Akamatsu H, Morishita M, Mori T, Yamaoka Y, Suenaga K, Soares RM, Bogado AN, Ivancovich A, Yamanaka N (2015) 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 D, Hartman G, Nelson R, Frederick RD, Concibido V, Narvel J, Cregan P (2007) Map location of the Rpp1 locus that confers resistance to soybean rust in soybean. Crop Sci 47:837–838. https://doi.org/10.2135/cropsci2006.07.0484
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
Ishiwata YI, Furuya J (2020) Evaluating the contribution of soybean rust-resistant cultivars to soybean production and the soybean market in Brazil: a supply and demand model analysis. Sustainability 12:1422. https://doi.org/10.3390/su12041422
Jubic LM, Saile S, Furzer OJ, El Kasmi F, Dangl JL (2019) Help wanted: helper NLRs and plant immune responses. Curr Opin Plant Biol 50:82–94. https://doi.org/10.1016/j.pbi.2019.03.013
Kawashima CG, Guimarães GA, Nogueira SR, MacLean D, Cook DR, Steuernagel B, Baek J, Bouyioukos C, do VA Melo B, Tristão G (2016) A pigeonpea gene confers resistance to Asian soybean rust in soybean. Nat Biotechnol 34:661–665. https://doi.org/10.1038/nbt.3554
Keim P, Olson TC, Shoemaker RC (1988) A rapid protocol for isolating soybean DNA. Soybean Genet Newsl 15:150–152
Kim K-S, Unfried JR, Hyten DL, Frederick RD, Hartman GL, Nelson RL, Song Q, Diers BW (2012) Molecular mapping of soybean rust resistance in soybean accession PI 561356 and SNP haplotype analysis of the Rpp1 region in diverse germplasm. Theor Appl Genet 125:1339–1352. https://doi.org/10.1007/s00122-012-1932-5
King ZR, Harris DK, Pedley KF, Song Q, Wang D, Wen Z, Buck JW, Li Z, Roger Boerma HR (2016) A novel Phakopsora pachyrhizi resistance allele (Rpp) contributed by PI 567068A. Theor Appl Genet 129(3):517–534. https://doi.org/10.1007/s00122-015-2645-3
Kourelis J, Van Der Hoorn RA (2018) Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30(2):285–299. https://doi.org/10.1105/tpc.17.00579
Lemos NG, e Braccini AdL, Abdelnoor RV, de Oliveira MCN, Suenaga K, Yamanaka N (2011) Characterization of genes Rpp2, Rpp4, and Rpp5 for resistance to soybean rust. Euphytica 182:53–64. https://doi.org/10.1007/s10681-011-0465-3
Li H (2011) A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27:2987–2993. https://doi.org/10.1093/bioinformatics/btr509
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
Lin F, Chhapekar SS, Vieira CC, Da Silva MP, Rojas A, Lee D, ... Nguyen HT (2022) Breeding for disease resistance in soybean: a global perspective. Theor Appl Genet 1–100. https://doi.org/10.1007/s00122-022-04101-3
Maphosa M, Talwana H, Tukamuhabwa P (2012) Enhancing soybean rust resistance through Rpp2, Rpp3 and Rpp4 pair wise gene pyramiding. Afr J Agric Res 7:4271–4277. https://doi.org/10.5897/AJAR12.1123
Marchal C, Michalopoulou VA, Zou Z, Cevik V, Sarris PF (2022) Show me your ID: NLR immune receptors with integrated domains in plants. Essays Biochem. https://doi.org/10.1042/EBC20210084
McHale LK, Haun WJ, Xu WW, Bhaskar PB, Anderson JE, Hyten DL, Gerhardt DJ, Jeddeloh JA, Stupar RM (2012) Structural variants in the soybean genome localize to clusters of biotic stress-response genes. Plant Physiol 159:1295–1308. https://doi.org/10.1104/pp.112.194605
McLean R, Byth D (1980) Inheritance of resistance to rust (Phakopsora pachyrhizi) in soybeans. Aust J Agric Res 31:951–956. https://doi.org/10.1071/AR9800951
Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283. https://doi.org/10.1016/j.cj.2015.01.001
Meyer JD, Silva DCG, Yang C, Pedley KF, Zhang C, van de Mortel M, Hill JH, Shoemaker RC, Abdelnoor RV, Whitham SA (2009) Identification and analyses of candidate genes for Rpp4-mediated resistance to Asian soybean rust in soybean. Plant Physiol 150:295–307. https://doi.org/10.1104/pp.108.134551
Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci 88:9828–9832. https://doi.org/10.1073/pnas.88.21.9828
Miles M, Frederick R, Hartman G (2006) Evaluation of soybean germplasm for resistance to Phakopsora pachyrhizi. Plant Health Prog 7:33. https://doi.org/10.1094/PHP-2006-0104-01-rs
Miles M, Morel W, Ray J, Smith J, Frederick RD, Hartman G (2008) Adult plant evaluation of soybean accessions for resistance to Phakopsora pachyrhizi in the field and greenhouse in Paraguay. Plant Dis 92:96–105. https://doi.org/10.1094/PDIS-92-1-0096
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(2):829–834. https://doi.org/10.2135/cropsci06.07.0462
OEC. Observatory of Economic Complexity (2020) https://oec.world/en/profile/hs92/21201/. Acessed 12 June 2020
Ouellette LA, Reid RW, Blanchard SG, Brouwer CR (2018) LinkageMapView — rendering high-resolution linkage and QTL maps. Bioinformatics 34:306–307. https://doi.org/10.1093/bioinformatics/btx576
Paul C, Frederick R, Hill C, Hartman GL, Walker DR (2015) Comparison of pathogenic variation among Phakopsora pachyrhizi isolates collected from the United States and international locations, and identification of soybean genotypes resistant to the US isolates. Plant Dis 99:1059–1069. https://doi.org/10.1094/PDIS-09-14-0989-re
Pedley KF, Pandey AK, Ruck A, Lincoln LM, Whitham SA, Graham MA (2019) Rpp1 encodes a ULP1-NBS-LRR protein that controls immunity to Phakopsora pachyrhizi in soybean. Mol Plant Microbe Interact 32:120–133. https://doi.org/10.1094/MPMI-07-18-0198-fi
Periyannan S, Milne RJ, Figueroa M, Lagudah ES, Dodds PN (2017) An overview of genetic rust resistance: from broad to specific mechanisms. PLoS Pathog 13:e1006380. https://doi.org/10.1371/journal.ppat.1006380
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. https://doi.org/10.1007/s00122-009-1036-z
Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP (2011) Integrative Genomics Viewer. Nat Biotechnol 29:24–26. https://doi.org/10.1038/nbt.1754
Rocha G, Alves D, Oliveira J, Brommonschenkel S (2016) Identification and mapping of resistance genes to Phakopsora pachyrhizi in soybean (Glycine max L.) accession PI 594767-A. Genet Mol Res 15:1–15. https://doi.org/10.4238/gmr.15038475
Santos JVM, Valliyodan B, Joshi T, Khan SM, Liu Y, Wang J, Vuong TD, de Oliveira MF, Marcelino-Guimarães FC, Xu D (2016) Evaluation of genetic variation among Brazilian soybean cultivars through genome resequencing. BMC Genomics 17:110. https://doi.org/10.1186/s12864-016-2431-x
Savary S, Willocquet L, Pethybridge SJ, Esker P, McRoberts N, Nelson A (2019) The global burden of pathogens and pests on major food crops. Nat Ecol Evol 3(3):430–439. https://doi.org/10.1038/s41559-018-0793-y
Silva DC, Yamanaka N, Brogin RL, Arias CA, Nepomuceno AL, Di Mauro AO, Pereira SS, Nogueira LM, Passianotto AL, Abdelnoor RV (2008) Molecular mapping of two loci that confer resistance to Asian rust in soybean. Theor Appl Genet 117:57–63. https://doi.org/10.1007/s00122-008-0752-0
Song QJ, Marek LF, Shoemaker RC, Lark KG, Concibido VC, Delannay X, Specht JE, Cregan PB (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109:122–128. https://doi.org/10.1007/s00122-004-1602-3
Song Q, Hyten DL, Jia G, Quigley CV, Fickus EW, Nelson RL, Cregan PB (2013) Development and evaluation of SoySNP50K, a high-density genotyping array for soybean. PLoS One 8:e54985. https://doi.org/10.1371/journal.pone.0054985
Song Q, Jenkins J, Jia G, Hyten DL, Pantalone V, Jackson SA, Schmutz J, Cregan PB (2016) Construction of high resolution genetic linkage maps to improve the soybean genome sequence assembly Glyma1. 01. BMC Genomics 17:33. https://doi.org/10.1186/s12864-015-2344-0
Torkamaneh D, Laroche J, Bastien M et al (2017) Fast-GBS: a new pipeline for the efficient and highly accurate calling of SNPs from genotyping-by-sequencing data. BMC Bioinformatics 18:1–7. https://doi.org/10.1186/s12859-016-1431-9
Torkamaneh D, Laroche J, Valliyodan B, O’Donoughue L, Cober E, Rajcan I, Abdelnoor RV, Sreedasyam A, Schmutz J, Nguyen HT, Belzile F (2019) Soybean haplotype map (GmHapMap): a universal resource for soybean translational and functional genomics. BioRxiv:534578. https://doi.org/10.1101/534578
Twizeyimana M, Hartman GL (2012) Pathogenic variation of Phakopsora pachyrhizi isolates on soybean in the United States from 2006 to 2009. Plant Dis 96:75–81. https://doi.org/10.1094/PDIS-05-11-0379
USDA. World agricultural production. 2022. https://apps.fas.usda.gov/psdonline/circulars/oilseeds.pdf. Acessed 14 July 2022
Viganó J, Braccini AL, Schuster I, Menezes VMPS (2018) Microsatellite molecular marker-assisted gene pyramiding for resistance to Asian soybean rust (ASR). Acta Sci Agron 40:e39619. https://doi.org/10.4025/actasciagron.v40i1.39619
Walker DR, Boerma H, Phillips D, Schneider R, Buckley J, Shipe E, Mueller J, Weaver D, Sikora E, Moore S (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, Phillips DV, Buck JW, Nelson RL, Boerma HR (2014) Soybean germplasm accession seedling reactions to soybean rust isolates from Georgia. Crop Sci 54:1433–1447. https://doi.org/10.2135/cropsci2013.09.0654
Wu X (2017) Genetic characterization of Rpp1-mediated Asian soybean rust resistance using in-depth transcriptomic and genomic analyses. University of Illinois, Thesis
Yamanaka N, Hossain MM (2019) Pyramiding three rust-resistance genes confers a high level of resistance in soybean (Glycine max). Plant Breed 138:686–695. https://doi.org/10.1111/pbr.12720
Yamanaka N, Yamaoka Y, Kato M, Lemos NG, Passianotto ALdL, dos 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. https://doi.org/10.1590/S1982-56762010000300003
Yamanaka N, Hossain MM, Yamaoka Y (2015) Molecular mapping of Asian soybean rust resistance in Chinese and Japanese soybean lines, Xiao Jing Huang, Himeshirazu, and Iyodaizu B. Euphytica 205:311–324. https://doi.org/10.1007/s10681-015-1377-4
Yamanaka N, Morishita M, Mori T, Muraki Y, Hasegawa M, Hossain MM, Yamaoka Y, Kato M (2016) The locus for resistance to Asian soybean rust in PI 587855. Plant Breed 135:621–626. https://doi.org/10.1111/pbr.12392
Yorinori JT, Paiva WM, Frederick RD, Costamilan LM, Bertagnolli PF, Hartman GE, Godoy CV, Nunes J Jr (2005) Epidemics of soybean rust (Phakopsora pachyrhizi) in Brazil and Paraguay from 2001 to 2003. Plant Dis 89:675–677. https://doi.org/10.1094/PD-89-0675
Acknowledgements
We would like to acknowledge Adriana Santos, Ana Maria Avelino, Allan Flausino, Marcia Kuwaraha, and Rogério Omura at Embrapa Soybean for providing technical support in greenhouse assays and genotyping support in the Laboratory of Plant Biotechnology and Laboratory of Molecular Genetics and Marker Assisted Selection. We would also like to acknowledge David Silva and Rafaella Bissi for helping in the phenotyping assays.
Funding
This work was funded by Brazilian Agricultural Research Corporation (EMBRAPA) (20.18.01.010.00.00) and National Council for the Improvement of Higher Education (CAPES) – Finance code 001 for a scholarship to Luciane Barros.
Author information
Authors and Affiliations
Contributions
Luciane Barros conducted and reported all mapping experiments and helped in writing the manuscript. Bruna Avelino helped in conducting all mapping experiments and the comparative testing of the level of resistance against pure pathotypes. Danielle Silva provided oversight for experiments, interpreted the results, and helped in writing the manuscript. Everton Ferreira designed the line graphs and helped in mapping and haplotype analysis. Carlos Arias provided crosses and populations, and revised the manuscript. Fernanda Castanho conducted the comparative testing of the level of resistance against pure pathotypes. Marcio Ferreira provided SoySNP6K Infinium Chips results. Valeria Lopes-Caitar processed the re-sequencing data to variant calling file. Silvana Marin oversighted SSR analyses. Ricardo Abdelnoor revised the manuscript and English language adequacy. Ivani Lopes helped in statistical interpretation and English language adequacy. Francismar Guimarães designed the project, supervised the study, approved funding, helped in writing and edited the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
The authors consented for the publication.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Barros, L.G., Avelino, B.B., da Silva, D.C.G. et al. Mapping of a soybean rust resistance in PI 594756 at the Rpp1 locus. Mol Breeding 43, 12 (2023). https://doi.org/10.1007/s11032-023-01358-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-023-01358-4