{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,9]],"date-time":"2026-07-09T04:35:01Z","timestamp":1783571701397,"version":"3.55.0"},"reference-count":44,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2025,6,29]],"date-time":"2025-06-29T00:00:00Z","timestamp":1751155200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the National Key Research and Development Program of China","award":["2021YFD1201103-01-05"],"award-info":[{"award-number":["2021YFD1201103-01-05"]}]},{"name":"the National Key Research and Development Program of China","award":["32301819"],"award-info":[{"award-number":["32301819"]}]},{"name":"the National Natural Science Foundation of China","award":["2021YFD1201103-01-05"],"award-info":[{"award-number":["2021YFD1201103-01-05"]}]},{"name":"the National Natural Science Foundation of China","award":["32301819"],"award-info":[{"award-number":["32301819"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Soybean frogeye leaf spot (FLS) disease has been reported globally and is caused by the fungus Cercospora sojina, which affects the growth, seed yield, and quality of soybean. Among the 15 physiological microspecies of C. sojina soybean in China, Race 7 is one of the main pathogenic microspecies. A few genes are involved in resistance to FLS, and they cannot meet the need to design molecular breeding methods for disease resistance. In this study, a soybean recombinant inbred line (RIL3613) population and a germplasm resource (GP) population were planted at two sites, Acheng (AC) and Xiangyang (XY). Phenotypic data on the percentage of leaf area diseased (PLAD) in soybean leaves were obtained via image recognition technology after the inoculation of seven physiological species and full onset at the R3 stage. Quantitative trait loci (QTLs) and quantitative trait nucleotides (QTNs) were mapped via linkage analysis and genome-wide association studies (GWASs), respectively. The resistance genes of FLS were subsequently predicted in the linkage disequilibrium region of the collocated QTN. We identified 114 QTLs and 18 QTNs in the RIL3613 and GP populations, respectively. A total of 14 QTN loci were colocalized in the two populations, six of which presented high phenotypic contributions. Through haplotype\u2013phenotype association analysis and expression quantification, three genes (Glyma.06G300100, Glyma.06G300600, and Glyma.13G172300) located near molecular markers AX-90524088 and AX-90437152 (QTNs) are associated with FLS Chinese Race 7, identifying them as potential candidate resistance genes. These results provide a theoretical basis for the genetic mining of soybean antigray spot No. 7 physiological species. These findings also provide a theoretical basis for understanding the genetic mechanism underlying FLS resistance in soybeans.<\/jats:p>","DOI":"10.3390\/plants14131988","type":"journal-article","created":{"date-parts":[[2025,6,30]],"date-time":"2025-06-30T05:00:37Z","timestamp":1751259637000},"page":"1988","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Fine Mapping of QTLs\/QTNs and Mining of Genes Associated with Race 7 of the Soybean Cercospora sojina by Combining Linkages and GWAS"],"prefix":"10.3390","volume":"14","author":[{"given":"Yanzuo","family":"Liu","sequence":"first","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Key Laboratory of Soybean Biology and Breeding\/Genetics, Ministry of Agriculture, 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, Key Laboratory of Soybean Biology and Breeding\/Genetics, Ministry of Agriculture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aitong","family":"Yu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Key Laboratory of Soybean Biology and Breeding\/Genetics, Ministry of Agriculture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuxi","family":"Liu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Key Laboratory of Soybean Biology and Breeding\/Genetics, Ministry of Agriculture, 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, Key Laboratory of Soybean Biology and Breeding\/Genetics, Ministry of Agriculture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yang","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Morden Agriculture and Ecological Environment, Heilongjiang University, Harbin 150080, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junjie","family":"Ding","sequence":"additional","affiliation":[{"name":"Jiamusi Branch, Heilongjiang Academy of Agricultural Sciences, Jiamusi 154007, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuzhen","family":"Zhang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Soybean Biology, Ministry of Education, Key Laboratory of Soybean Biology and Breeding\/Genetics, Ministry of Agriculture, 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, Key Laboratory of Soybean Biology and Breeding\/Genetics, Ministry of Agriculture, 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, Key Laboratory of Soybean Biology and Breeding\/Genetics, Ministry of Agriculture, Northeast Agricultural University, Harbin 150030, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,6,29]]},"reference":[{"key":"ref_1","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_2","first-page":"660","article-title":"The inheritance of resistance to frog-eye leaf spot of soybeans","volume":"42","author":"Athow","year":"1952","journal-title":"Phytopathology"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Copping, L.G., Green, M.B., and Rees, R.T. (1992). Management of foliar fungal diseases in soybean in Brazil. Pest Management in Soybean, Springer.","DOI":"10.1007\/978-94-011-2870-4"},{"key":"ref_4","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_5","doi-asserted-by":"crossref","unstructured":"Soares, A.P.G., Guillin, E.A., Borges, L.L., Silva, A.C.T.d., Almeida, \u00c1.M.R.d., Grijalba, P.E., Gottlieb, A.M., Bluhm, B.H., and Oliveira, L.O.d. (2015). More Cercospora species infect soybeans across the Americas than meets the eye. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0133495"},{"key":"ref_6","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_7","first-page":"870","article-title":"Advances in Cercospora sojina physiological races and inheritance of resistance to soybean frogeye leaf spot","volume":"25","author":"Xiao","year":"2024","journal-title":"J. Plant Genet. Resour."},{"key":"ref_8","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_9","doi-asserted-by":"crossref","first-page":"764","DOI":"10.1094\/Phyto-72-764","article-title":"Two Genes for Resistance to Race 5 of Cercospora sojina in Soybeans","volume":"72","author":"Phillips","year":"1982","journal-title":"Phytopathology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1046\/j.1439-0523.2001.00563.x","article-title":"Molecular mapping of a new gene for resistance to frogeye leaf spot of soya bean in \u2018Peking\u2019","volume":"120","author":"Yang","year":"2001","journal-title":"Plant Breed."},{"key":"ref_11","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_12","first-page":"1132","article-title":"Association analysis of resistance of soybean to Cercospora sojina Hara Race 10 based on SSR markers","volume":"43","author":"Liang","year":"2021","journal-title":"Chin. J. Oil Crop Sci."},{"key":"ref_13","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_14","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_15","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_16","doi-asserted-by":"crossref","first-page":"222","DOI":"10.1071\/CP21128","article-title":"SNP-bin linkage analysis and genome-wide association study of plant height in soybean","volume":"73","author":"Wang","year":"2022","journal-title":"Crop Pasture Sci."},{"key":"ref_17","first-page":"41","article-title":"A QTL mapping analysis of main yield traits in soybean","volume":"35","author":"Yao","year":"2014","journal-title":"J. South China Agric. Univ."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Zhang, K., Liu, S., Li, W., Liu, S., Li, X., Fang, Y., Zhang, J., Wang, Y., Xu, S., and Zhang, J. (2018). Identification of QTNs controlling seed protein content in soybean using multi-locus genome-wide association studies. Front. Plant Sci., 9.","DOI":"10.3389\/fpls.2018.01690"},{"key":"ref_19","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_20","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_21","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1111\/jipb.13839","article-title":"The SlWRKY42\u2013SlMYC2 module synergistically enhances tomato saline\u2013alkali tolerance by activating the jasmonic acid signaling and spermidine biosynthesis pathway","volume":"67","author":"Liu","year":"2025","journal-title":"J. Integr. Plant Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2551","DOI":"10.1105\/tpc.014167","article-title":"The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis","volume":"15","author":"Mengiste","year":"2003","journal-title":"Plant Cell"},{"key":"ref_23","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_24","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_25","first-page":"175","article-title":"Advance on methodology of QTL mapping for plants","volume":"22","author":"Gao","year":"2000","journal-title":"Hereditas"},{"key":"ref_26","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_27","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1007\/s00122-020-03756-0","article-title":"Fine mapping QTL and mining genes for protein content in soybean by the combination of linkage and association analysis","volume":"134","author":"Li","year":"2021","journal-title":"Theor. Appl. Genet."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Sun, M., Zhao, T., Liu, S., Han, J., Wang, Y., Zhao, X., Li, Y., Teng, W., Zhan, Y., and Han, Y. (2024). QTL Detection of Salt Tolerance at Soybean Seedling Stage Based on Genome-Wide Association Analysis and Linkage Analysis. Plants, 13.","DOI":"10.3390\/plants13162283"},{"key":"ref_29","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_30","doi-asserted-by":"crossref","unstructured":"Xiong, X., Li, J., Su, P., Duan, H., Sun, L., Xu, S., Sun, Y., Zhao, H., Chen, X., and Ding, D. (2023). Genetic dissection of maize (Zea mays L.) chlorophyll content using multi-locus genome-wide association studies. BMC Genom., 24.","DOI":"10.1186\/s12864-023-09504-0"},{"key":"ref_31","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_32","doi-asserted-by":"crossref","unstructured":"Hong, H., Li, M., Chen, Y., Wang, H., Wang, J., Guo, B., Gao, H., Ren, H., Yuan, M., and Han, Y. (2022). Genome-wide association studies for soybean epicotyl length in two environments using 3VmrMLM. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.1033120"},{"key":"ref_33","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_34","doi-asserted-by":"crossref","unstructured":"Wei, N., Zhang, S., Liu, Y., Wang, J., Wu, B., Zhao, J., Qiao, L., Zheng, X., Wang, J., and Zheng, J. (2022). Genome-wide association study of coleoptile length with Shanxi wheat. Front. Plant Sci., 13.","DOI":"10.3389\/fpls.2022.1016551"},{"key":"ref_35","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_36","first-page":"97","article-title":"Soybean variety resource resistant to Cercospora sojina race 7: Mining of elite alleles","volume":"36","author":"Hongjiao","year":"2020","journal-title":"Chin. Agric. Sci. Bull."},{"key":"ref_37","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_38","first-page":"402","article-title":"Excavation the resistance locus to Cercospora sojina Hara race 12 in soybean by association analysis","volume":"35","author":"Dong","year":"2016","journal-title":"Soybean Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/S1369-5266(00)00199-0","article-title":"The R2R3-MYB gene family in Arabidopsis thaliana","volume":"4","author":"Stracke","year":"2001","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1093\/genetics\/153.1.427","article-title":"Maize R2R3 Myb genes: Sequence analysis reveals amplification in the higher plants","volume":"153","author":"Rabinowicz","year":"1999","journal-title":"Genetics"},{"key":"ref_41","first-page":"1265","article-title":"The roles of MYB transcription factors on plant defense responses and its molecular mechanism","volume":"30","author":"Liu","year":"2008","journal-title":"Hereditas"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Pal, D., De, K., Shanks, C.M., Feng, K., Yates, T.B., Morrell-Falvey, J., Davidson, R.B., Parks, J.M., and Muchero, W. (2022). Core cysteine residues in the Plasminogen-Apple-Nematode (PAN) domain are critical for HGF\/c-MET signaling. Commun. Biol., 5.","DOI":"10.1038\/s42003-022-03582-8"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"De, K., Pal, D., Shanks, C.M., Yates, T.B., Feng, K., Jawdy, S.S., Hassan, M.M., Prabhakar, P.K., Yang, J.Y., and Chapla, D. (2023). The Plasminogen-Apple-Nematode (PAN) domain suppresses JA\/ET defense pathways in plants. bioRxiv.","DOI":"10.1101\/2023.06.15.545202"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Freitas, C.D.T., Costa, J.H., Germano, T.A., Rocha, R.d.O., Ramos, M.V., and Bezerra, L.P. (2024). Class III plant peroxidases: From classification to physiological functions. Int. J. Biol. Macromol., 263.","DOI":"10.1016\/j.ijbiomac.2024.130306"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/14\/13\/1988\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:01:26Z","timestamp":1760032886000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/14\/13\/1988"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6,29]]},"references-count":44,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2025,7]]}},"alternative-id":["plants14131988"],"URL":"https:\/\/doi.org\/10.3390\/plants14131988","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,29]]}}}