Abstract
Maize rough dwarf disease (MRDD) is a devastating viral disease that causes considerable yield losses in maize worldwide. Identifying quantitative trait loci underlying resistance to MRDD is important for genetic improvement of maize. In this study, 184 elite maize inbred lines from modern breeding programs were evaluated in three years to identify QTLs for MRDD resistance using 3072 single-nucleotide polymorphisms (SNPs) via genome-wide association analysis. The analysis revealed abundant phenotypic diversity in the studied population. All tested maize inbred lines were divided into two subpopulations based on a Bayesian model, and the linkage disequilibrium (LD) level differed among chromosomes, with an intra-chromosomal average of 1,000–1,500 kb. After correction for multiple testing, 21 SNPs were identified for MRDD resistance in different years as well as for BLUPs (the best linear unbiased predictions) of MRDD resistance based on the MLM model, one SNP of PZE-101245575 was stably possessed the most promising association. Several SNPs were located in or close to previously reported quantitative trait loci for MRDD resistance. The significant SNPs identified in this study will be helpful for further understanding the genetic basis of MRDD resistance, and might facilitate the pyramiding of favorable alleles for high resistance to MRDD in future marker-assisted selection schemes in maize.
Similar content being viewed by others
References
Ali F, Yan J (2012) Disease resistance in maize and the role of molecular breeding in defending against global threat. J Integr Plant Biol 54(3):134–151
Bai F, Yan J, Qu Z, Zhang H, Xu J, Ye M, Shen D (2002) Phylogenetic analysis reveals that a dwarfing disease on different cereal crops in China is due to rice black streaked dwarf virus (RBSDV). Virus Genes 25(2):201–206
Bonamico N, Balzarini M, Arroyo A, Ibañez M, Díaz D, Salerno J, Di Renzo M (2010) Association between microsatellites and resistance to Mal de Río Cuarto in maize by discriminant analysis. Phyton Int J Exp Bot 79:31
Bonamico N, Di Renzo M, Ibañez M, Borghi M, Díaz D, Salerno J, Balzarini M (2012) QTL analysis of resistance to Mal de Río Cuarto disease in maize using recombinant inbred lines. J Agr Sci 150(05):619–629
Bradbury P, Zhang Z, Kroon D, Casstevens T, Ramdoss Y, Buckler E (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633
Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172(2):1165–1177
Cardon L, Bell J (2001) Association study designs for complex diseases. Nat Rev Genet 2(2):91–99
Chan EKF, Rowe HC, Corwin JA, Joseph B, Kliebenstein DJ (2011) Combining Genome-Wide Association Mapping and Transcriptional Networks to Identify Novel Genes Controlling Glucosinolates in Arabidopsis thaliana. PLoS Biol 9(8):e1001125
Chen Y, Li X, Xiao M, Li M, Yuan S, Wang X, Zhang S (2006) Genetic variation in sixty-four maize inbred lines in relation to maize rough dwarf virus. Acta Agr Sin 12:1848–1854
Chen Y, Meng Q, Yuan J (2008) Identification of the molecular markers linked to the MRDV-resistance locus in maize using SSR-BSA technique. Jiangsu J Agr Sci 24(5):590–594
Ching A, Caldwell K, Jung M, Dolan M, Smith O, Tingey S, Morgante M, Rafalski A (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3(1):19
Chinnusamy V, Gong Z, Zhu J-K (2008) Nuclear RNA export and its importance in abiotic stress responses of plants. In: Nuclear pre-mRNA Processing in Plants. Springer, p 235–255
Collard BCY, Jahufer MZZ, Brouwer J, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142(1):169–196
Devlin B, Roeder K (2004) Genomic control for association studies. Biometrics 55(4):997–1004
Di Renzo MA, Bonamico NC, Díaz D, Salerno JC, Ibanez M, Gesumaría J (2002) Inheritance of resistance to Mal de Río Cuarto (MRC) disease in Zea mays. J Agr Sci 139(01):47–53
Di Renzo MA, Bonamico NC, Díaz DG, Ibañez M, Faricelli ME, Balzarini M, Salerno JC (2004) Microsatellite markers linked to QTL for resistance to Mal de Rio Cuarto disease in Zea mays L. J Agri Sci 142:289–295
Dovas C, Eythymiou K, Katis N (2004) First report of maize rough dwarf virus (MRDV) on maize crops in Greece. Plant Pathol 53(2):238
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620
Excoffier L, Laval G, Schneider S (2005) ARLEQUIN version 3.01: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Fang S, Yu J, Feng J, Han C, Li D, Liu Y (2001) Identification of rice black-streaked dwarf fijivirus in maize with rough dwarf disease in China. Arch Virol 146(1):167–170
Ganal MW, Durstewitz G, Polley A, Berard A, Buckler ES, Charcosset A, Clarke JD, Graner E-M, Hansen M, Joets J (2011) A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS ONE 6(12):e28334
Gupta P, Rustgi S, Kulwal P (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57(4):461–485
Hao Z, Li X, Xie C, Weng J, Li M, Zhang D, Liang X, Liu L, Liu S, Zhang S (2011) Identification of functional genetic variations underlying drought tolerance in maize using SNP markers. J Integr Plant Biol 53(8):641–652
Hao D, Chao M, Yin Z, Yu D (2012a) Genome-wide association analysis detecting significant single nucleotide polymorphisms for chlorophyll and chlorophyll fluorescence parameters in soybean (Glycine max) landraces. Euphytica 186:919–931
Hao D, Cheng H, Yin Z, Cui S, Zhang D, Wang H, Yu D (2012b) Identification of single nucleotide polymorphisms and haplotypes associated with yield and yield components in soybean (Glycine max) landraces across multiple environments. Theor Appl Genet 124:447–458
Hardy O, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Not 2(4):618–620
Harpaz I (1959) Needle transmission of a new maize virus. Nature 184:77–78
Holland J, Nyquist W, Cervantes-Martínez C (2003) Estimating and interpreting heritability for plant breeding: An update. Plant Breeding Rev 22:9–112
Kazama D, Itakura M, Kurusu T, Mitsuda N, Ohme-Takagi M, Tada Y (2013) Identification of chimeric repressors that confer salt and osmotic stress. Tol Arab Plants 2:769–785
Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR, Oropeza-Rosas MA, Zwonitzer JC, Kresovich S, McMullen MD, Ware D (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43(2):163–168
Li X, Yan W, Agrama H, Jia L, Shen X, Jackson A, Moldenhauer K, Yeater K, McClung A, Wu D (2011) Mapping QTLs for improving grain yield using the USDA rice mini-core collection. Planta 234(2):347–361
Li H, Peng Z, Yang X, Wang W, Fu J, Wang J, Han Y, Chai Y, Guo T, Yang N (2012a) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45(1):43–50
Li Q, Yang X, Xu S, Cai Y, Zhang D, Han Y, Li L, Zhang Z, Gao S, Li J (2012b) Genome-wide association studies identified three independent polymorphisms associated with α-tocopherol content in maize kernels. PLoS ONE 7(5):e36807
Liu K, Muse S (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21(9):2128
Luan J, Wang F, Li Y, Zhang B, Zhang J (2012) Mapping quantitative trait loci conferring resistance to rice black-streaked virus in maize (Zea mays L.). Theor Appl Genet 125:781–791
Miao H, Tian L, Lu Y, Di D, Chen X (2005) Simple severity classification standard of maize rough dwarf disease. Plant Prot 31:255
Murray M, Thompson W (1980) Rapid isolation of high molecular weight plant DNA. Nucl Acids Res 8(19):4321–4326
Phumichai C, Chunwongse J, Jampatong S, Grudloyma P, Pulam T, Doungchan W, Wongkaew A, Kongsiri N (2012) Detection and integration of gene mapping of downy mildew resistance in maize inbred lines though linkage and association. Euphytica 187:369–379
Poland JA, Bradbury PJ, Buckler ES, Nelson RJ (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc Nat Acad Sci 108(17):6893–6898
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Riedelsheimer C, Czedik-Eysenberg A, Grieder C, Lisec J, Technow F, Sulpice R, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012a) Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat Genet 44(2):217–220
Riedelsheimer C, Lisec J, Czedik-Eysenberg A, Sulpice R, Flis A, Grieder C, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012b) Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proc Nat Acad Sci 109(23):8872–8877
Segura V, Vilhjálmsson BJ, Platt A, Korte A, Seren Ü, Long Q, Nordborg M (2012) An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations. Nat Genet 44(7):825–830
Sheen J (1998) Mutational analysis of protein phosphatase 2C involved in abscisic acid signal transduction in higher plants. Proc Nat Acad Sci 95:975–980
Shi L, Hao Z, Weng J, Xie C, Liu C, Zhang D, Li M, Bai L, Li X, Zhang S (2012a) Identification of a major quantitative trait locus for resistance to maize rough dwarf virus in a Chinese maize inbred line X178 using a linkage map based on 514 gene-derived single nucleotide polymorphisms. DOI, Mol Breeding. doi:10.1007/s11032-11011-19652-11030
Shi M, Xue L, Liang K, Huang D, Huang X, Hu J, Jiang J, Ruan F, Chen G, Lu H, Cheng Y, Chen X (2012b) QTL Mapping for resistance to rough dwarf disease with GY220/1145 combination in maize (Zea mays L.). Jiangsu J Agr Sci 28(2):259–264
Smigocki A, Neal J Jr, McCanna I, Douglass L (1993) Cytokinin-mediated insect resistance in Nicotiana plants transformed with the ipt gene. Plant Mol Biol 23:325–335
Stich B, Melchinger A (2010) An introduction to association mapping in plants. CAB Rev 5:1–9
Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Nat Acad Sci 100:9440–9445
Strigens A, Freitag NM, Gilbert X, Grieder C, Riedelsheimer C, Schrag TA, Messmer R, Melchinger AE (2013) Association mapping for chilling tolerance in elite flint and dent maize inbred lines evaluated in growth chamber and field experiments. Plant Cell Environ 36(10):1871–1887
Tao Y, Liu Q, Wang H, Zhang Y, Huang X, Wang B, Lai J, Ye J, Liu B, Xu M (2013) Identification and fine-mapping of a QTL, qMrdd1, that confers recessive resistance to maize rough dwarf disease. BMC Plant Biol 13(1):145
Van Inghelandt D, Reif JC, Dhillon BS, Flament P, Melchinger AE (2011) Extent and genome-wide distribution of linkage disequilibrium in commercial maize germplasm. Theor Appl Genet 123(1):11–20
Van Inghelandt D, Melchinger AE, Martinant JP, Stich B (2012) Genome-wide association mapping of flowering time and northern corn leaf blight (Setosphaeria turcica) resistance in a vast commercial maize germplasm set. BMC Plant Biol 12(1):56
Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era—concepts and misconceptions. Nat Rev Genet 9:255–266
Wang A, Zhao D, Chen Z, Wang J, Shao X, Wei G (2000) Studies on genetic basis and recurrent selection effect of inbred line maize Resistance to MRDV. Maize Sci 8:80–82
Wang F, Qin G, Sui Z, Wang Z, Yu J, Zhang J (2006) Improved method for assaying maize plant resistance to maize rough dwarf disease by artificial inoculation and real-time RT-PCR. Eur J Plant Pathol 116(4):289–300
Wang H, Smith KP, Combs E, Blake T, Horsley RD, Muehlbauer GJ (2012) Effect of population size and unbalanced data sets on QTL detection using genome-wide association mapping in barley breeding germplasm. Theor Appl Genet 124(1):111–124
Wisser RJ, Kolkman JM, Patzoldt ME, Holland JB, Yu J, Krakowsky M, Nelson RJ, Balint-Kurti PJ (2011) Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene. Proc Nat Acad Sci 108(18):7339–7344
Würschum T (2012) Mapping QTL for agronomic traits in breeding populations. Theor Appl Genet 125:201–210
Xing Y, Zhang Q (2010) Genetic and molecular bases of rice yield. Ann Rev Plant Biol 61:421–442
Xu Y, Crouch J (2008) Marker-assisted selection in plant breeding: from publications to practice. Crop Sci 48(2):391–407
Xue L, Zhang D, Xu L, Jin M, Peng C, Xu C (2011) Mining and analyzing genetic diversity for maize rough dwarf disease resistant gerplasms and its application in maize breeding. Acta Agr Sin 37(12):2123–2129
Yan J, Shah T, Warburton M, Buckler E, McMullen M, Crouch J (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4(12):e8451
Yan J, Yang X, Shah T, Sa´nchez-Villeda H, Li J, Warburton M, Zhou Y, Crouch JH, Xu Y (2010) High-throughput SNP genotyping with the GoldenGate assay in maize. Mol Breeding 25(3):441–451
Yan J, Warburton M, Crouch J (2011) Association mapping for enhancing maize (Zea mays L.) genetic improvement. Crop Sci 51:433
Yang X, Yan J, Shah T, Warburton M, Li Q, Li L, Gao Y, Chai Y, Fu Z, Zhou Y (2010) Genetic analysis and characterization of a new maize association mapping panel for quantitative trait loci dissection. Theor Appl Genet 121:417–431
Yang X, Gao S, Xu S, Zhang Z, Prasanna BM, Li L, Li J, Yan J (2011) Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol Breeding 28(4):511–526
Yu J, Buckler E (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotech 17(2):155–160
Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38(2):203–208
Zambrano JL, Jones MW, Brenner E, Francis DM, Tomas A, Redinbaugh MG (2014) Genetic analysis of resistance to six virus diseases in a multiple virus-resistant maize inbred line. Theor Appl Genet. doi:10.1007/s00122-014-2263-5
Zhang H, Chen J, Lei J, Adams MJ (2001) Sequence analysis shows that a dwarfing disease on rice, wheat and maize in China is caused by Rice black-streaked dwarf virus. Eur J Plant Pathol 107(5):563–567
Acknowledgments
This work was supported by the National Basic Research Program of China (973 Program 2011CB100106),the Natural Science Foundation of Jiangsu Province, China (BK20141241), the Scientific and Technological Program of Jiangsu Province, China (BE2011303, BE2012335, BY2014082), and the Scientific and Technological Platform Construction Program of Nantong City, China (CP12012002).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hao, D., Cheng, Y., Chen, G. et al. Identification of significant single nucleotide polymorphisms for resistance to maize rough dwarf disease in elite maize (Zea mays L.) inbred lines. Euphytica 203, 109–120 (2015). https://doi.org/10.1007/s10681-014-1277-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10681-014-1277-z