{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T17:47:34Z","timestamp":1785433654687,"version":"3.56.0"},"reference-count":53,"publisher":"MDPI AG","issue":"14","license":[{"start":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T00:00:00Z","timestamp":1783468800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"crossref","award":["32301819"],"award-info":[{"award-number":["32301819"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"crossref"}]},{"award":["32301819"],"award-info":[{"award-number":["32301819"]}],"id":[{"id":"https:\/\/ror.org\/01h0zpd94","id-type":"ROR","asserted-by":"publisher"}]},{"name":"National Key Research and Development Program of China","award":["2021YFD1201103-01-05"],"award-info":[{"award-number":["2021YFD1201103-01-05"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Soybean (Glycine max) is a major economic and food crop whose yield is severely affected by frogeye leaf spot (FLS), caused by Cercospora sojina. Current knowledge of resistance genes remains insufficient for effective molecular breeding. In this study, a recombinant inbred line (RIL) population derived from a cross between the resistant parent, Henong 60 (H60), and the susceptible parent, Dongnong L13 (DN L13), was evaluated under field conditions in Acheng (AC) and Xiangyang (XY). Plants were artificially inoculated with physiological race 7 of C. sojina, and disease severity at the R3 growth stage was recorded. Genotyping using the SoySNP660K chip yielded 54,836 high-quality single-nucleotide polymorphism (SNP) markers. A genome-wide association study (GWAS) was performed using the 3VmrMLM model by integrating dual-environment phenotypic data, and four quantitative trait nucleotides (QTNs) significantly associated with resistance to FLS were identified on chromosomes 8 (1), 17 (1), and 20 (2). By the analysis of genomic annotation, functional enrichment, metabolic pathway analyses, haplotype\u2013phenotype association and quantitative real-time PCR (qRT-PCR), Glyma.20G155700 and Glyma.17G070500 are intended to be candidate genes related to soybean resistance to race 7 of FLS. The findings of this study provide insights into the genetic mechanisms underlying resistance to FLS in soybean. The identified molecular markers and candidate genes may provide useful resources for marker-assisted breeding and the development of disease-resistant germplasm.<\/jats:p>","DOI":"10.3390\/plants15142106","type":"journal-article","created":{"date-parts":[[2026,7,8]],"date-time":"2026-07-08T15:40:09Z","timestamp":1783525209000},"page":"2106","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Genome-Wide Association Study Identifies QTNs and Candidate Genes Conferring Resistance to Soybean Frogeye Leaf Spot Race 7"],"prefix":"10.3390","volume":"15","author":[{"given":"Yanzuo","family":"Liu","sequence":"first","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo","family":"Hu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tianqi","family":"Xing","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pengfei","family":"Xu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuzhen","family":"Zhang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Xia","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hailong","family":"Ning","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,7,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1016\/S0261-2194(91)80134-2","article-title":"Yield losses in soybeans from frogeye leaf spot caused by Cercospora sojina","volume":"10","author":"Dashiell","year":"1991","journal-title":"Crop Prot."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"14","DOI":"10.2135\/cropsci2007.08.0432","article-title":"Frogeye leaf spot of soybean: A review and proposed race designations for isolates of Cercospora sojina Hara","volume":"48","author":"Mian","year":"2008","journal-title":"Crop Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1094\/PHYTO-09-12-0229-R","article-title":"Mating-type distribution and genetic diversity of Cercospora sojina populations on soybean from Arkansas: Evidence for potential sexual reproduction","volume":"103","author":"Kim","year":"2013","journal-title":"Phytopathology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1094\/Phyto-71-334","article-title":"Cercospora sojina race 5: A threat to soybeans in the southeastern United States","volume":"71","author":"Phillips","year":"1981","journal-title":"Phytopathology"},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Yorinori, J.T. (1992). Management of foliar fungal diseases in soybean in Brazil. Pest Management in Soybean, Springer.","DOI":"10.1007\/978-94-011-2870-4_18"},{"key":"ref_6","first-page":"315","article-title":"The study of Cercospora sojina Hara races in Heilongjiang Province","volume":"7","author":"Huo","year":"1988","journal-title":"Soybean Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"14","DOI":"10.5897\/JPBCS2020.0938","article-title":"QTL mapping for resistance to Cercospora sojina in Essex Forrest soybean (Glycine max L.) lines","volume":"13","author":"McAllister","year":"2021","journal-title":"J. Plant Breed. Crop Sci."},{"key":"ref_8","first-page":"660","article-title":"The inheritance of resistance to frogeye leaf spot of soybean","volume":"42","author":"Athow","year":"1952","journal-title":"Phytopathology"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"332","DOI":"10.2135\/cropsci1965.0011183X000500040013x","article-title":"Inheritance of resistance to race 2 of Cercospora sojina in soybeans","volume":"5","author":"Probst","year":"1965","journal-title":"Crop Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1687","DOI":"10.2135\/cropsci1999.3961687x","article-title":"Molecular mapping of the Rcs3 gene for resistance to frogeye leaf spot in soybean","volume":"39","author":"Mian","year":"1999","journal-title":"Crop Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.ygeno.2018.01.004","article-title":"Genome-wide association mapping for seed protein and oil contents using a large panel of soybean accessions","volume":"111","author":"Li","year":"2019","journal-title":"Genomics"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Li, X., Zhang, X., Zhu, L., Bu, Y., Wang, X., Zhang, X., Zhou, Y., Wang, X., Guo, N., and Qiu, L. (2019). Genome-wide association study of four yield-related traits at the R6 stage in soybean. BMC Genet., 20.","DOI":"10.1186\/s12863-019-0737-9"},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Lu, W., Sui, M., Zhao, X., Jia, H., Han, D., Yan, X., and Han, Y. (2022). Genome-wide identification of candidate genes underlying soluble sugar content in vegetable soybean (Glycine max L.) via association and expression analysis. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.930639"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"722","DOI":"10.1111\/jipb.12323","article-title":"Detection and fine-mapping of SC7 resistance genes via linkage and association analysis in soybean","volume":"57","author":"Yan","year":"2015","journal-title":"J. Integr. Plant Biol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Zhang, Q., Sun, T., Wang, J., Fei, J., Liu, Y., Liu, L., and Wang, P. (2023). Genome-wide association study and high-quality gene mining related to soybean protein and fat. BMC Genom., 24.","DOI":"10.1186\/s12864-023-09687-6"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Zhao, X., Jiang, H., Feng, L., Qu, Y., Teng, W., Qiu, L., Zheng, H., Han, Y., and Li, W. (2019). Genome-wide association and transcriptional studies reveal novel genes for unsaturated fatty acid synthesis in a panel of soybean accessions. BMC Genom., 20.","DOI":"10.1186\/s12864-019-5449-z"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Sun, M., Na, C., Jing, Y., Cui, Z., Li, N., Zhan, Y., Teng, W., Li, Y., Li, W., and Zhao, X. (2022). Genome-wide association analysis and gene mining of resistance to China race 1 of frogeye leaf spot in soybean. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.867713"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s00122-023-04359-1","article-title":"Genome-wide association analysis of resistance to frogeye leaf spot China race 7 in soybean based on high-throughput sequencing","volume":"136","author":"Na","year":"2023","journal-title":"Theor. Appl. Genet."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Fang, Y., Liu, S., Dong, Q., Zhang, K., Tian, Z., Li, X., Li, W., Qi, Z., Wang, Y., and Tian, X. (2020). Linkage analysis and multi-locus genome-wide association studies identify QTNs controlling soybean plant height. Front. Plant Sci., 11.","DOI":"10.3389\/fpls.2020.00009"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1016\/j.cj.2020.07.004","article-title":"Detection of QTL and QTN and candidate genes for oil content in soybean using a combination of four-way-RIL and germplasm populations","volume":"8","author":"Li","year":"2020","journal-title":"Crop J."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Liu, Y., Hu, B., Yu, A., Liu, Y., Xu, P., Wang, Y., Ding, J., Zhang, S., Li, W.-X., and Ning, H. (2025). Fine mapping of QTLs\/QTNs and mining of genes associated with race 7 of the soybean Cercospora sojina by combining linkages and GWAS. Plants, 14.","DOI":"10.3390\/plants14131988"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"77","DOI":"10.5433\/1679-0359.2016v37n1p77","article-title":"The combined effects of temperature and leaf wetness periods on soybean frogeye leaf spot intensity","volume":"37","author":"Camera","year":"2016","journal-title":"Semin. Ci\u00eanc. Agr\u00e1r. Londrina"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Hartman, G.L., Rupe, J.C., Sikora, E.J., Domier, L.L., Davis, J.A., and Steffey, K.L. (2015). Compendium of Soybean Diseases and Pests, American Phytopathological Society Press. [5th ed.].","DOI":"10.1094\/9780890544754"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1094\/PHP-2009-0512-03-RS","article-title":"Characterization and survival of Cercospora sojina in Ohio","volume":"10","author":"Cruz","year":"2009","journal-title":"Plant Health Prog."},{"key":"ref_25","first-page":"987","article-title":"Biology and epidemiology of Cercospora sojina","volume":"69","author":"Singh","year":"1985","journal-title":"Plant Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"16236","DOI":"10.1038\/s41598-026-46975-z","article-title":"Modeling the Environment-Related Risk of Frogeye Leaf Spot (Cercospora sojina) in Soybean Across the United States","volume":"16","author":"Allen","year":"2026","journal-title":"Sci. Rep."},{"key":"ref_27","unstructured":"Guterres, C.W., Navarini, L., and Seidel, G. (2026, April 02). El Ni\u00f1o and La Ni\u00f1a effects on Cercospora blight epidemics in southern Brazil soybean, Cultivar Grandes Culturas Magazine, Available online: https:\/\/revistacultivar.com\/articles\/el-nino-and-la-nina-in-cercospora-blight-in-soybeans."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Gu, X., Huang, S., Zhu, Z., Ma, Y., Yang, X., Yao, L., Gao, X., Zhang, M., Liu, W., and Qiu, L. (2021). Genome-wide association of single nucleotide polymorphism loci and candidate genes for frogeye leaf spot (Cercospora sojina) resistance in soybean. BMC Plant Biol., 21.","DOI":"10.1186\/s12870-021-03366-y"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1007\/s00438-022-01986-z","article-title":"Genome-wide association study reveals novel loci and a candidate gene for resistance to frogeye leaf spot (Cercospora sojina) in soybean","volume":"298","author":"McDonald","year":"2023","journal-title":"Mol. Genet. Genom."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Pham, A.T., Harris, D.K., Buck, J., Hoskins, A., Serrano, J., Abdel-Haleem, H., Cregan, P., Song, Q., Boerma, H.R., and Li, Z. (2015). Fine mapping and characterization of candidate genes that control resistance to Cercospora sojina K. Hara in two soybean germplasm accessions. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0126753"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Han, Z., Ke, H., Li, X., Peng, R., Zhai, D., Xu, Y., Wu, L., Wang, W., and Cui, Y. (2023). Detection of epistasis interaction loci for fiber quality-related trait via 3VmrMLM in upland cotton. Front. Plant Sci., 14.","DOI":"10.3389\/fpls.2023.1250161"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1016\/j.molp.2022.06.002","article-title":"IIIVmrMLM: The R and C++ tools associated with 3VmrMLM, a comprehensive GWAS method for dissecting quantitative traits","volume":"15","author":"Li","year":"2022","journal-title":"Mol. Plant"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Zhang, J., Wang, S., Wu, X., Han, L., Wang, Y., and Wen, Y. (2022). Identification of QTNs, QTN-by-environment interactions and genes for yield-related traits in rice using 3VmrMLM. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.995609"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"He, L., Wang, H., Sui, Y., Miao, Y., Jin, C., and Luo, J. (2022). Genome-wide association studies of five free amino acid levels in rice. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.1048860"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Niu, H., Kuang, M., Huang, L., Shang, H., Yuan, Y., and Ge, Q. (2023). Lint percentage and boll weight QTLs in three excellent upland cotton (Gossypium hirsutum): ZR014121, CCRI60, and EZ60. BMC Plant Biol., 23.","DOI":"10.1186\/s12870-023-04147-5"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1111\/pbi.12249","article-title":"Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean","volume":"13","author":"Sonah","year":"2015","journal-title":"Plant Biotechnol. J."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Wang, J., Hu, B., Jing, Y., Hu, X., Guo, Y., Chen, J., Liu, Y., Hao, J., Li, W.-X., and Ning, H. (2022). Detecting QTL and candidate genes for plant height in soybean via linkage analysis and GWAS. Front. Plant Sci., 12.","DOI":"10.3389\/fpls.2021.803820"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Chen, Y., Yue, X.L., Feng, J.Y., Gong, X., Zhang, W.J., Zuo, J.F., and Zhang, Y.M. (2024). Identification of QTNs, QTN-by-environment interactions, and their candidate genes for salt tolerance related traits in soybean. BMC Plant Biol., 24.","DOI":"10.1186\/s12870-024-05021-8"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1007\/s11103-025-01576-8","article-title":"Detection of genes associated with soybean protein content using a genome-wide association study","volume":"115","author":"Yu","year":"2025","journal-title":"Plant Mol. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1111\/j.1399-3054.2008.01149.x","article-title":"Overexpression of a rice defense-related F-box protein gene OsDRF1 in tobacco improves disease resistance through potentiation of defense gene expression","volume":"134","author":"Cao","year":"2008","journal-title":"Physiol. Plant."},{"key":"ref_41","first-page":"503","article-title":"Progress in functional characterization of F-box protein family","volume":"29","author":"Wu","year":"2002","journal-title":"Prog. Biochem. Biophys."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Piisil\u00e4, M., Keceli, M., Brader, G., Jakobson, L., J\u00f5esaar, I., Sipari, N., Kollist, H., Palva, E., and Kariola, T. (2015). The F-box protein MAX2 contributes to resistance to bacterial phytopathogens in Arabidopsis thaliana. BMC Plant Biol., 15.","DOI":"10.1186\/s12870-015-0434-4"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1007\/s11240-013-0405-0","article-title":"Down-regulation of S-adenosylmethionine decarboxylase genes results in reduced plant length, pollen viability, and abiotic stress tolerance","volume":"116","author":"Chen","year":"2014","journal-title":"Plant Cell Tissue Organ Cult."},{"key":"ref_44","first-page":"1125","article-title":"Mechanism of F-box protein family in plant resistance response to environmental stress","volume":"26","author":"Jia","year":"2018","journal-title":"Chin. J. Eco-Agric."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1007\/s001220051352","article-title":"Differential accumulation of the S-adenosylmethionine decarboxylase transcript in rice seedlings in response to salt and drought stresses","volume":"100","author":"Li","year":"2000","journal-title":"Theor. Appl. Genet."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Stefanowicz, K., Lannoo, N., Zhao, Y., Eggermont, L., Van Hove, J., Al Atalah, B., and Van Damme, E.J.M. (2016). Glycan-binding F-box protein from Arabidopsis thaliana protects plants from Pseudomonas syringae infection. BMC Plant Biol., 16.","DOI":"10.1186\/s12870-016-0905-2"},{"key":"ref_47","first-page":"107","article-title":"Identification of S-adenosy lmethionine decarboxylase gene family involved in polyamines synthesis in peach and its response to abiotic stresses","volume":"46","author":"Hou","year":"2024","journal-title":"J. Southwest Univ. Nat. Sci. Ed."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1016\/j.jmb.2015.06.020","article-title":"Remaining mysteries of molecular biology: The role of polyamines in the cell","volume":"427","author":"Campbell","year":"2015","journal-title":"J. Mol. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"102317","DOI":"10.1016\/j.pmpp.2024.102317","article-title":"Regulation of the polyamine pool in plants: Metabolic implications and stress mitigation, with emphasis on microbial influence","volume":"132","author":"Roy","year":"2024","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"144230","DOI":"10.1016\/j.gene.2019.144230","article-title":"Polyamine homeostasis in tomato biotic\/abiotic stress cross-tolerance","volume":"727","author":"Tsaniklidis","year":"2020","journal-title":"Gene"},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Yi, Q., Park, M.J., Vo, K.T.X., and Jeon, J.S. (2024). Polyamines in plant\u2013pathogen interactions: Roles in defense mechanisms and pathogenicity with applications in fungicide development. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms252010927"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Ma, S., Niu, H., Liu, C., Zhang, J., Hou, C., and Wang, D. (2013). Expression stabilities of candidate reference genes for RT-qPCR under different stress conditions in soybean. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0075271"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Bansal, R., Mittapelly, P., Cassone, B.J., Mamidala, P., Redinbaugh, M.G., and Michel, A. (2015). Recommended reference genes for quantitative PCR analysis in soybean have variable stabilities during diverse biotic stresses. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0134890"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/14\/2106\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,10]],"date-time":"2026-07-10T04:13:34Z","timestamp":1783656814000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/14\/2106"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,7,8]]},"references-count":53,"journal-issue":{"issue":"14","published-online":{"date-parts":[[2026,7]]}},"alternative-id":["plants15142106"],"URL":"https:\/\/doi.org\/10.3390\/plants15142106","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,8]]}}}