Abstract
Both plant height (PH) and ear height (EH) are key agronomic traits in maize that are associated with plant lodging resistance and population density. To explore the genetic basis for PH and EH in maize, we conducted a genome-wide association study (GWAS) based upon 1.49 × 106 single nucleotide polymorphisms (SNPs) identified following the sequencing of 80 backbone inbred maize lines in Jilin Province. By comparing genotypic data and these two traits of interest, we identified 27 total SNPs significantly associated with PH and EH (P < 0.000001). Of these SNPs, 12 were significantly associated with PH and were found on chromosomes 1, 3, 4, 6, 7, and 9, accounting for 25.8% of the phenotypic variability for this trait. The remaining 15 SNPs were significantly linked with EH and were located on chromosomes 1, 2, 4, 6, 7, 8, 9, and 10, accounting for 30% of the phenotypic variability for this trait. Within a mean linkage disequilibrium (LD) distance of 9.7 kb from these SNP loci, we identified 5 candidate genes associated with PH, with one of these candidate genes harboring a significant SNP. Similarly, we identified 12 candidate genes associated with EH, of which 3 harbored significant SNPs. We then isolated RNA from 8 different inbred maize lines from this GWAS study cohort and assessed the expression of these candidate genes of interest via quantitative real-time PCR (qRT-PCR). Through this analysis, we were able to verify that there were significant differences in the expression of these four SNP-harboring candidate genes in plants with a range of EH and PH phenotypes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andrade FH, Uhart SA, Frugone MI (1993) Intercepted radiation at flowering and kernel number in maize: shade versus plant density effects. Crop Sci 33(3):92–97. https://doi.org/10.2135/cropsci1993.0011183X003300030013x
Beavis WD, Smith OS, Grant D et al (1994) Identification of quantitative trait loci using a small sample of top crossed and F4 progeny from maize. Crop Sci 34(4). https://doi.org/10.2135/cropsci1994.0011183X003400040010x
Berke TG, Rocheford TR (1995) Quantitative trait loci for flowering, plant and ear height, and kernel traits in maize. Crop Sci 35(6). https://doi.org/10.2135/cropsci1995.0011183X003500060004x
Bittner-Eddy PD, Crute IR, Holub EB et al (2010) RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J 21(2):177–188. https://doi.org/10.1046/j.1365-313x.2000.00664.x
Borba AR, Serra TS, Górska A (2018) Synergistic binding of bHLH transcription factors to the promoter of the maize NADP-ME gene used in C4 photosynthesis is based on an ancient code found in the ancestral C3 state. Mol Biol Evol 35(7):1690–1705. https://doi.org/10.1093/molbev/msy060
Buckler ES et al (2009) The genetic architecture of maize flowering time. Science 325:714–718. https://doi.org/10.1126/science.1174276
Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66(1):94–116. https://doi.org/10.1111/j.1365-313x.2010.04459.x
Frascaroli E, Cane MA, Landi P et al (2007) Classical genetic and quantitative trait loci analyses of heterosis in a maize hybrid between two elite inbred lines. Genetics 176(1):625–644. https://doi.org/10.1534/genetics.106.064493
Gilad Y, Pritchard JK, Thornton K (2009) Characterizing natural variation using next-generation sequencing technologies. Trends Genet 25:463–471. https://doi.org/10.1016/j.tig.2009.09.003
Harper LC, Schaeffer ML, Thistle J et al (2011) The maizeGDB genome browser tutorial: one example of database outreach to biologists via video. Database 2011:bar016. https://doi.org/10.1093/database/bar016
He K, Xu S, Li J (2013) BAK1 directly regulates brassinosteroid perception and BRI1 activation. J Integr Plant Biol 55(12):1264–1270. https://doi.org/10.1111/jipb.12122
Ku L, Zhang J, Guo S, Liu HY, Zhao RF, Chen YH (2012) Integrated multiple population analysis of leaf architecture traits in maize (Zea mays L.). J Exp Bot 63:261–274. https://doi.org/10.1093/jxb/err277
Kusmec A, Schnable PS (2018) FarmCPUpp: efficient large-scale genomewide association studies. Plant Direct 2(4):e00053. https://doi.org/10.1002/pld3.53
Lambert RJ, Johnson RR (1978) Leaf angle, tassel morphology, and the performance of maize hybrids1. Crop Sci 18:499–502. https://doi.org/10.2135/cropsci1978.0011183X001800030037x
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Li Q, Li Y, Yang Z et al (2013) QTL mapping for plant height and ear height by using multiple related RIL populations in maize. Acta Agron Sin 39(9):1521–1529. https://doi.org/10.3724/SP.J.1006.2013.01521
Li C, Li Y, Shi Y, Song Y, Zhang D, Buckler ES, Zhang Z, Wang T, Li Y (2015) Genetic control of the leaf angle and leaf orientation value as revealed by ultra-high density maps in three connected maize populations. PLoS One 10(3):e0121624. https://doi.org/10.1371/journal.pone.0121624
Li X, Zhou Z, Ding J et al (2016) Combined linkage and association mapping reveals QTL and candidate genes for plant and ear height in maize. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.00833
Liu C, Weng J, Zhang D, Zhang X, Yang X, Shi L, Meng Q, Yuan J, Guo X, Hao Z, Xie C, Li M, Ci X, Bai L, Li X, Zhang S (2014) Genome-wide association study of resistance to rough dwarf disease in maize. Eur J Plant Pathol 139:205–216. https://doi.org/10.1007/s10658-014-0383-z
Liu X, Huang M, Fan B, Buckler ES, Zhang Z (2016) Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet 12:e1005767. https://doi.org/10.1371/journal.pgen.1005767
Lu S, Zhang M, Zhang Z et al (2018) Screening and verification of genes associated with leaf angle and leaf orientation value in inbred maize lines. PLoS One 13(12):e0208386. https://doi.org/10.1371/journal.pone.0208386
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325. https://doi.org/10.1093/nar/8.19.4321
Nordborg M, Weigel D (2008) Next-generation genetics in plants. Nature 456:720–723. https://doi.org/10.1038/nature07629
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. https://doi.org/10.1086/519795
Sangoi L, Gracietti MA, Rampazzo C et al (2002) Response of Brazilian maize hybrids from different eras to changes in plant density. Field Crop Res 79(1):39–51. https://doi.org/10.1016/S0378-4290(02)00124-7
Sheehan D, Meade G, Foley VM et al (2001) Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem J 360(1):1–16. https://doi.org/10.1042/bj3600001
Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, Rocheford TR, McMullen M, Holland JB, Buckler ES (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43:159–162. https://doi.org/10.1038/ng.746
Varshney RK, Nayak SN, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27:522–530. https://doi.org/10.1016/j.tibtech.2009.05.006
Wang Y, Yao J, Zhang Z, Zheng Y (2006) The comparative analysis based on maize integrated QTL map and meta-analysis of plant height QTLs. Chin Sci Bull 51(18):2219–2230. https://doi.org/10.1007/s11434-006-2119-8
Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38(16):e164. https://doi.org/10.1093/nar/gkq603
Wei C, Li H, Tian M et al (2017) Research progress for F-box protein family function in arabidopsis thaliana. Acta Bot Boreal-Occident Sin 37(11):210–218. https://doi.org/10.7606/j.issn.1000-4025.2017.11.2300
Weng J, Xie C, Hao Z et al (2011) Genome-wide association study identifies candidate genes that affect plant height in Chinese elite maize (Zea mays L.) inbred lines. PLoS One 6(12):e29229. https://doi.org/10.1371/journal.pone.0029229
Wu J, Liu C, Shi Y et al (2005) QTL analysis of plant height and ear height in maize under different water regimes. J Plant Gene Resour 6(3):266–271 Doi:CNKI:SUN:ZWYC.0.2005-03-004
Yang X, Lu M, Zhang S et al (2008) Maize plant and ear height QTL mapping. Hereditas 30(11):97–106 Doi:CNKI:SUN:YCZZ.0.2008-11-021
Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160. https://doi.org/10.1016/j.copbio.2006.02.003
Zhang Y, Li Y, Wang Y et al (2010) Stability of QTL across environments and QTL-by-environment interactions for plant and ear height in maize. Agric Sci China 9:1400–1412. https://doi.org/10.1016/S1671-2927(09)60231-5
Zhang C, Zhao L, Zhao H et al (2011) Advances in plant protein kinase. Biotechnol Bull 10:23–29 Doi:CNKI:SUN:SWJT.0.2011-10-004
Zheng K, Li Y, Lv H et al (2015) QTL mapping of plant height and ear height in maize. Jiangsu Agric Sci 43(5):73–75 Doi:CNKI:SUN:JSNY.0.2015-05-018
Zhou Z, Zhang C, Zhou Y, Hao Z, Wang Z, Zeng X, di H, Li M, Zhang D, Yong H, Zhang S, Weng J, Li X (2016) Genetic dissection of maize plant architecture with an ultra-high density bin map based on recombinant inbred lines. BMC Genomics 17(1):178. https://doi.org/10.1186/s12864-016-2555-z
Zhu J, Yang CJ, Wang J (2009) Real-time fluorescent quantitative PCR and application in scientific research. Biotechnol Bull 2:73–76. https://doi.org/10.1002/9780470686812.ch1
Acknowledgments
This study was funded by the Agricultural Science and Technology Innovation Program of Jilin Province-Postdoctoral foundation(c92071509) and Human Resources Development of Human Resources and Social Security Department of Jilin Province. We also thank editor and reviewers for their valuable suggestions and careful corrections.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Elliosha Hajari
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lu, S., Li, M., Zhang, M. et al. Genome-Wide Association Study of Plant and Ear Height in Maize. Tropical Plant Biol. 13, 262–273 (2020). https://doi.org/10.1007/s12042-020-09258-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12042-020-09258-z