Abstract
Gibberella ear rot (GER) caused by Fusarium graminearum (teleomorph Gibberella zeae), is one of the most devastating diseases in maize that not only severely reduces grain yield but also contaminates the kernels with potent mycotoxins which is harmful to livestock and humans. Identification of stable quantitative trait loci (QTL) and candidate genes conferring resistance is a promising strategy in resistance breeding programs for the disease. Here, the ten times intermated B73 × Mo17-doubled haploid (IBM Syn10 DH) population comprising a total of 298 diverse maize inbred lines were subjected to phenotypic evaluation in a 2-year field test across two environments, and the IBM Syn10 DH population were employed to detect QTL across multiple environments using an ultra-high-density bin map. Ten QTL were detected on chromosomes 1, 2, 3, 6, 7, 8, and 9, respectively. Of them, a major QTL on chromosome 7, named qGRfg7, could explain 33.26% of the phenotypic variation. Based on fine-mapping strategy, we narrowed down the interested region into 91 kb, flanked by two developed Indel markers. A predicted gene in the mapped region, encoding a lipopolysaccharide-binding protein (LBP), is suggested to be a candidate gene conferring resistance to GER disease. These results will facilitate the breeding process for GER resistance by marker-assisted selection (MAS) in maize.
Similar content being viewed by others
References
Ali ML, Taylor JH, Jie L, Sun G, William M, Kasha KJ, Reid LM, Pauls KP (2005) Molecular mapping of QTLs for resistance to Gibberella ear rot, in corn, caused by Fusarium graminearum. Genome 48:521–533. https://doi.org/10.1139/g05-014
Chen JF, Ding JQ, Li HM, Li ZM, Sun XD, Li JJ, Wang RX, Dai XD, Dong HF, Song WB, We C, Xia ZL, Wu JY (2012) Detection and verification of quantitative trait loci for resistance to Fusarium ear rot in maize. Mol Breed 30:1649–1656. https://doi.org/10.1007/s11032-012-9748-1
Chen JF, Shrestha R, Ding JQ, Zheng HJ, Mu CH, Wu JY, Mahuku G (2016) Genome-wide association study and QTL mapping reveal genomic loci associated with Fusarium ear rot resistance in tropical maize germplasm. G3: Genes|Genomes|Genetics 6:3803–3815. https://doi.org/10.1534/g3.116.034561
Chen Q, Song J, Du WP, Xu LY, Jiang Y, Zhang J, Xiang XL, Yu GR (2017) Identification, mapping, and molecular marker development for Rgsr8.1: a new quantitative trait locus conferring resistance to Gibberella stalk rot in maize (Zea mays L.). Front Plant Sci 8:1355. https://doi.org/10.3389/fpls.2017.01355
Clair DA (2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 48:247–268. https://doi.org/10.1016/j.pbi.2009.12.010
Collard BY, Jahufer MZ, Brouwer JB, Pang EK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196. https://doi.org/10.1007/s10681-005-1681-5
Dell’Acqua M, Gatti DM, Pea G, Cattonaro F, Coppens F, Magris G, Hlaing AL, Aung HH, Nelissen H, Baute J, Frascaroli E, Churchill G, Inze D, Morgante M, Pé ME (2015) Genetic properties of the MAGIC maize population: a new platform for high definition QTL mapping in Zea mays. Genome Biol 16:167. https://doi.org/10.1186/s13059-015-0716-z
Ding JQ, Wang XM, Chander S, Yan JB, Li JS (2008) QTL mapping of resistance to Fusarium ear rot using a RIL population in maize. Mol Breed 22:395–403. https://doi.org/10.1007/s11032-008-9184-4
Duan CX, Qin ZH, Yang ZH, Li WX, Sun SL, Zhu ZD, Wang XM (2016) Identification of pathogenic Fusarium spp. causing maize ear rot and potential mycotoxin production in China. Toxins 8, 186. https://doi.org/10.3390/toxins8060186
Geng ZY, Zhu W, Su H, Zhao Y, Zhang KQ, Yang JK (2014) Recent advances in genes involved in secondary metabolite synthesis, hyphal development, energy metabolism and pathogenicity in Fusarium graminearum (teleomorph Gibberella zeae). Biotech Adva 32:390–402. https://doi.org/10.1016/j.biotechadv.2013.12.007
Hurni S, Scheuermann D, Krattinger SG, Kessel B, Wicker T, Herren G, Fitze MN, Breen J, Presterl T, Ouzunova M, Keller B (2015) The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. Proc Natl Acad Sci U S A 112:8780–8785. https://doi.org/10.1073/pnas.1502522112
Hussain T, Tausend P, Graham G, Ho J (2007) Registration of IBM2 SYN10 doubled haploid mapping population of maize. J Plant Regist 1:81. https://doi.org/10.3198/jpr2005.11.0414crs
Kebede AZ, Woldemariam T, Reid LM, Harris LJ (2016) Quantitative trait loci mapping for Gibberella ear rot resistance and associated agronomic traits using genotyping-by-sequencing in maize. Theor Appl Genet 129:17–29. https://doi.org/10.1007/s00122-015-2600-3
Kebede AZ, Johnston A, Schneiderman D, Bosnich W, Harris LJ (2018) Transcriptome profiling of two maize inbreds with distinct responses to Gibberella ear rot disease to identify candidate resistance genes. BMC Genomics 19:131. https://doi.org/10.1186/s12864-018-4513-4
Knapp S, Stroup W, Ross W (1985) Exact confidence intervals for heritability on a progeny mean basis 1. Crop Sci 25:192–194. https://doi.org/10.2135/cropsci1985.0011183X002500010046x
Kou YJ, Wang SP (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:1–5. https://doi.org/10.1016/j.pbi.2009.12.010
Liu HJ, Niu YC, Gonzalez-Portilla PJ, Zhou HK, Wang LY, Zuo T, Qin C, Tai SS, Jansen C, Shen YO, Lin HJ, Lee M, Ware D, Zhang ZZ, Lübberstedt T, Pan GT (2015) An ultra-high-density map as a community resource for discerning the genetic basis of quantitative traits in maize. BMC Genomics 16:1078. https://doi.org/10.1186/s12864-015-2242-5
Liu YJ, Guo YL, Ma CY, Zhang DF, Wang C, Yang Q, Xu ML (2016) Transcriptome analysis of maize resistance to Fusarium graminearum. BMC Genomics 17:477. https://doi.org/10.1186/s12864-016-2780-5
Liu HJ, Zhang L, Wang JC, Li CS, Zeng X, Xie SP, Zhang YH, Sisi Liu HSL, Wang JH, Lee M, Lübberstedt T, Zhao GW (2017) Quantitative trait locus analysis for deep-sowing germination ability in the maize IBM Syn10 DH population. Front Plant Sci 8:813. https://doi.org/10.3389/fpls.2017.00813
Liu M, Tan XL, Yang Y, Liu P, Zhang XX, Zhang YC, Wang L, Hu Y, Ma LL, Li ZL, Zhang YL, Zou CY, Lin HJ, Gao SB, Lee M, Lübberstedt T, Pan GT, Shen YO (2019) Analysis of the genetic architecture of maize kernel size traits by combined linkage and association mapping. Plant Biotechnol J 18(1):1–309. 1-15. https://doi.org/10.1111/pbi.13188
Lizasa S, Lizasa E, Watanabe K, Nagano Y (2017) Transcriptome analysis reveals key roles of AtLBR-2 in LPS-induced defense responses in plants. BMC Genomics 18:995. https://doi.org/10.1186/s12864-017-4372-4
Ma CY, Ma XN, Yao LS, Liu YJ, Du FL, Yang XH, Xu ML (2017) qRfg3, a novel quantitative resistance locus against Gibberella stalk rot in maize. Theor Appl Genet 130:1723–1734. https://doi.org/10.1007/s00122-017-2921-5
Martin M, Miedaner T, Dhillon BS, Ufermann U, Kessel B, Ouzunova M, Schipprack W, Melchinger AE (2011) Colocalization of QTL for Gibberella ear rot resistance and low mycotoxin contamination in early European maize. Crop Sci 51:1935–1945. https://doi.org/10.2135/cropsci2010.11.0664
Martin M, Dhillon BS, Miedaner T, Melchinger AE (2012) Inheritance of resistance to Gibberella ear rot and deoxynivalenol contamination in five flint maize crosses. Plant Breed 131:28–32. https://doi.org/10.1111/j.1439-0523.2011.01908.x
Maschietto V, Colombi C, Pirona R, Pea G, Strozzi F, Marocco A, Rossini L (2017) QTL mapping and candidate genes for resistance to Fusarium ear rot and fumonisin contamination in maize. BMC Plant Biol 17:20. https://doi.org/10.1186/s12870-017-0970-1
Mesterházy Á, Lemmens M, Reid LM (2012) Breeding for resistance to ear rots caused by Fusarium spp. in maize – a review. Plant Breed 131:1–19. https://doi.org/10.1111/j.1439-0523.2011.01936.x
Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:139. https://doi.org/10.3389/fpls.2013.00139
Pérez-Brito D, Jeffers D, González-de-León D, Khairallah M, Cortés-Cruz M, Velázquez-Cardelas G, Azpíroz-Rivero S, Srinivasan G (2001) QTL mapping of Fusarium moniliforme ear rot resistance in highland maize, Mexico. Agrociencia 35:181–196
Ranf S (2016) Immune sensing of lipopolysaccharide in plants and animals: same but different. PLoS Pathog 9:1–7. https://doi.org/10.1371/journal.ppat.1005596
Reid LM, Nicol RW, Ouellet T, Savard M, Miller JD, Young JC, Stewart DW, Schaafsma AW (1999) Interaction of Fusarium graminearum and F. moniliforme in maize ears: disease progress, fungal biomass, and mycotoxin accumulation. Phytopathol 89:1028–1037. https://doi.org/10.1094/PHYTO.1999.89.11.1028
Robertson-Hoyt LA, Jines MP, Balint-Kurti PJ, Kleinschmidt CE, White DG, Payne GA, Maragos CM, Molnar TL, Holland JB (2006) QTL mapping for Fusarium ear rot and fumonisin contamination resistance in two maize populations. Crop Sci 46:1734–1743. https://doi.org/10.2135/cropsci2005.12-0450
Szalma SJ, Hostert BM, LeDeaux JR, Stuber CW, Holland JB (2007) QTL mapping with near-isogenic lines in maize. Theor Appl Genet 114:1211–1228. https://doi.org/10.1007/s00122-007-0512-6
Tao YF, Jiang L, Liu QQ, Zhang Y, Zhang R, Ingvardsen CR, Frei UK, Wang BB, Lai JS, Lübberstedt T, Xu ML (2013) Combined linkage and association mapping reveals candidates for Scmv1, a major locus involved in resistance to sugarcane mosaic virus (SCMV) in maize. BMC Plant Biol 13:162. https://doi.org/10.1186/1471-2229-13-162
Tuinstra MR, Ejeta G, Goldsbrough PB (1997) Heterogenous inbred family (HIF) analysis: a method for developing near-isogenic lines that differ at quantitative trait loci. Theor Appl Genet 95:1005–1011. https://doi.org/10.1007/s001220050654
Vigier B, Reid LM, Dwyer LM, Stewart DW, Sinha RC, Arnason JT, Butler G (2001) Maize resistance to Gibberella ear rot: symptoms, deoxynivalenol, and yield. Can J Plant Pathol 23:99–105. https://doi.org/10.1080/07060660109506915
Wang H, Nussbaum-Wagler T, Li BL, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF (2005) The origin of the naked grains of maize. Nature 436:714–719. https://doi.org/10.1038/nature03863
Wang S, Basten CJ, Zeng ZB (2012) Windows QTL cartographer 2.5. In: Department of Statistics. North Carolina State University, Raleigh http://st.atgen.ncsu.edu/qtllcart/WQTLCart.htm. Accessed 15 March 2014
Weidenborner M (2001) Foods and fumonisins. Eur Food Res Technol 212:262–273. https://doi.org/10.1007/s002170000259
Xiang K, Zhang ZM, Reid LM, Zhu XY, Yuan GS, Pan GT (2010) A meta-analysis of QTL associated with ear rot resistance in maize. Maydica 55:281–290. https://doi.org/10.3198/jpr2009.06.0350crmp
Yang Q, Yin GM, Guo YL, Zhang DF, Chen SJ, Xu ML (2010) A major QTL for resistance to Gibberella stalk rot in maize. Theor Appl Genet 121:673–687. https://doi.org/10.1007/s00122-010-1339-0
Yang JY, Yan RX, Roy A, Xu D, Poisson J, Zhang Y (2014) The I-TASSER Suite: protein structure and function prediction. Nat Methods 12:7–8. https://doi.org/10.1038/nmeth.3213
Yang Q, Balint-Kurtil P, Xu ML (2017) Quantitative disease resistance: dissection and adoption in maize. Mol Plant 10:402–413. https://doi.org/10.1016/j.molp.2017.02.004
Yu J, Holland JB, McMullen MD, Buckler ES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178:539–551. https://doi.org/10.1534/genetics.107.074245
Yuan J, Ali ML, Taylor J, Liu J, Sun G, Liu W, Masilimany P, Gulati-Sakhuja A, Pauls KP (2008) A guanylyl cyclase-like gene is associated with Gibberella ear rot resistance in maize (Zea mays L.). Theor App Genet 116(4):465–479. https://doi.org/10.1007/s00122-007-0683-1
Zhang F, Wan XQ, Pan GT (2006) QTL mapping of Fusarium moniliforme ear rot resistance in maize.1. Map construction with microsatellite and AFLP markers. J Appl Genet 47:9–15. https://doi.org/10.1007/BF03194593
Zhang DF, Liu YJ, Guo YL, Yang Q, Ye JR, Chen SJ, Xu ML (2012) Fine-mapping of qRfg2, a QTL for resistance to Gibberella stalk rot in maize. Theor Appl Genet 124:585–596. https://doi.org/10.1007/s00122-011-1731-4
Zhang YL, Liang TH, Chen M, Zhang YC, Wang T, Lin HJ, Rong TZ, Zou CY, Liu P, Lee M, Pan GT, Shen YO, Lübberstedt T (2019) Genetic dissection of stalk lodging-related traits using an IBM Syn10 DH population in maize across three environments (Zea mays L.). Mol Genet Genomics. https://doi.org/10.1007/s00438-019-01576-6
Zuo WL, Chao Q, Zhang N, Ye JR, Tan GQ, Li BL, Xing YX, Zhang BQ, Liu HJ, Fengler KA, Zhao J, Zhao XR, Chen YS, Lai JS, Yan JB, Xu ML (2015) A maize wall-associated kinase confers quantitative resistance to head smut. Nat Genet 47:151–157. https://doi.org/10.1038/ng.3170
Funding
This study was funded by the National Transgenic Major Project of China (2019ZX08010-002), the National Natural Science Foundation of China (31471513), and the Science and Technology Research Program of Sichuan (2018JY0170 and 2020YJ0407).
Author information
Authors and Affiliations
Contributions
G. Y and Z. Z designed and carried out the experiment, analyzed the data, and wrote the manuscript; B. C, H. P, and Q. Z contributed to plant materials management and phenotypic evaluation; Y. L, K. X, and L. L prepared the figures; C. Z and H. L contributed for QTL detection; H. D and G. P contributed for critically reading this manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 167 kb)
Rights and permissions
About this article
Cite this article
Yuan, G., Chen, B., Peng, H. et al. QTL mapping for resistance to ear rot caused by Fusarium graminearum using an IBM Syn10 DH population in maize. Mol Breeding 40, 91 (2020). https://doi.org/10.1007/s11032-020-01158-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-020-01158-0