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A SNP-Based High-Density Genetic Map Reveals Reproducible QTLs for Tassel-Related Traits in Maize (Zea mays L.)

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Abstract

The tassel architecture of maize (Zea mays L.), which plays an important role in F1 hybrid seed production and yield performance, is genetically controlled by quantitative trait loci (QTLs). Here, we constructed a high-density SNP-based genetic map using an F2 population containing 148 individuals. This genetic map included 7613 SNPs whose average genetic distance was 0.19 cM. On account of the F2 population, we detected 14 QTLs responsible for tassel branch number (TBN), tassel weight (TW), central spike length (CSL), and meristem length (ML); eight of these QTLs demonstrated a relatively high level of phenotypic variation explanation (PVE) (PVE ≥ 10%), at a high level of significance. qTW-2 was a major QTL (LOD = 10.11 and PVE = 28.82%), and this QTL and qTBN-2 shared the same region, indicating a possible pleiotropic effect. An F2:3 population was developed to further verify QTLs in the F2 population. Finally, qTBN-5, qTW-2 and qCSL_N-10 were detected reproducibly. To help screen potential candidate genes, we chose 12 genes within the regions of qTBN-5, qML-6, qCSL_N-7 and qTW-2 and that were possibly involved in tassel morphogenesis according to Gene Ontology (GO) annotation analysis and performed quantitative real-time polymerase chain reaction (qRT-PCR). The expression of eight of the 12 genes was significantly (P < 0.05) or extremely significantly different (P < 0.01) between parents of the F2 population during the young tassel development stage, suggesting that those eight were possible candidate genes. These results provide insights into the genetic mechanisms controlling tassel architecture and will benefit both tassel-related QTL fine mapping and causal gene cloning in maize.

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Abbreviations

SNP:

Single Nucleotide Polymorphism

QTL:

quantitative trait locus

TBN:

tassel branch number

TW:

tassel weight

CSL_T:

central spike length (from top branch to tip of central spikelet)

CSL_N:

central spike length (from the tip of central spike to the non- branching node present below the lowermost primary branch)

ML:

meristem length

PVE:

phenotypic variation explanation

SLAF-seq:

Specific-Locus Amplified Fragment Sequencing

SD:

standard deviation.

RIL:

recombinant inbred line

qRT-PCR:

Quantitative real-time PCR

ADD:

additive effect

LOD:

logarithm of odds.

LD:

linkage disequilibrium

CTAB:

cetyl-trimethylammonium bromide

DOM:

dominant effect

References

  • Berke TG, Rocheford TR (1999) Quantitative trait loci for tassel traits in maize. Crop Sci 39:1439–1443

    Google Scholar 

  • Bolduc N, Yilmaz A, Mejia-Guerra MK, Morohashi K, O'Connor D, Grotewold E, Hake S (2012) Unraveling the KNOTTED1 regulatory network in maize meristems. Genes Dev 26:1685–1690

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bommert P, Lunde C, Nardmann J, Vollbrecht E, Running M, Jackson D, Hake S, Werr W (2005) thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132:1235–1245

    CAS  PubMed  Google Scholar 

  • Brewbaker JL (2015) Diversity and genetics of tassel branch numbers in maize. Crop Sci 55:65–78

    Google Scholar 

  • Brown PJ, Upadyayula N, Mahone GS, Tian F, Bradbury PJ, Myles S, Holland JB, Flint-Garcia S, McMullen MD, Buckler ES, Rocheford TR (2011) Distinct genetic architectures for male and female inflorescence traits of maize. PLoS Genet 7:e1002383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castro-Álvarez FF, William M, Bergvinson DJ, García-Lara S (2015) Genetic mapping of QTL for maize weevil resistance in a RIL population of tropical maize. Theor Appl Genet 128:411–419

    PubMed  Google Scholar 

  • Chen ZL, Wang BB, Dong XM, Liu H, Ren LH, Chen J, Hauck A, Song WB, Lai JS (2014) An ultra-high density bin-map for rapid QTL mapping for tassel and ear architecture in a large F2 maize population. BMC Genomics 15:433

    PubMed  PubMed Central  Google Scholar 

  • Chen ZJ, Yang C, Tang DG, Zhang L, Zhang L, Qu JT, Liu J (2017) Dissection of the genetic architecture for tassel branch number by QTL analysis in two related populations in maize. J Integr Agric 16:1432–1442

    Google Scholar 

  • Chuck G, Whipple C, Jackson D, Hake S (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137:1243–1250

    CAS  PubMed  Google Scholar 

  • Chuck GS, Brown PJ, Meeley R, Hake S (2014) Maize SBP-box transcription factors unbranched2 and unbranched3 affect yield traits by regulating the rate of lateral primordia initiation. Proc Natl Acad Sci 111:18775–18780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duvick DN, Cassman KG (1999) Post–green revolution trends in yield potential of temperate maize in the north-Central United States. Crop Sci 39:1622–1630

    Google Scholar 

  • Fang L et al (2017) Genomic analyses in cotton identify signatures of selection and loci associated with fiber quality and yield traits. Nat Genet 49:1089–1098

    CAS  PubMed  Google Scholar 

  • Gallavotti A, Long JA, Stanfield S, Yang X, Jackson D, Vollbrecht E, Schmidt RJ (2010) The control of axillary meristem fate in the maize ramosa pathway. Development 137:2849–2856

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galli M, Liu QJ, Moss BL, Malcomber S, Li W, Gaines C, Federici S, Roshkovan J, Meeley R, Nemhauser JL, Gallavotti A (2015) Auxin signaling modules regulate maize inflorescence architecture. Proc Natl Acad Sci 112:13372–13377

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao SB, Zhao MJ, Lan H, Zhang ZM (2007) Identification of QTL associated with tassel branch number and total tassel length in maize. Hereditas 29:1013–1017

    CAS  PubMed  Google Scholar 

  • Geraldi IO, Miranda Filho JB, Vencovsky R (1978) Estimation of genetic parameters of tassel characters in maize (Zea mays L.) and breeding perspectives. Relatorio Cientifico-Escola Superior de Agricultura Luiz de Queiroz Inst de Genetica (Brazil) no. 11

  • Hunter RB, Daynard TB, Hume DJ, Tanner JW, Curtis JD, Kannenberg LW (1969) Effect of tassel removal on grain yield of corn (Zea mays L.). Crop Sci 9:405–406

    Google Scholar 

  • Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugenics 12:172–175

    Google Scholar 

  • Lambert RJ, Johnson RR (1978) Leaf angle, tassel morphology, and the performance of maize hybrids. Crop Sci 18:499–502

    Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754–1760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu DY, Ma CX, Hong WG, Huang L, Liu M, Liu H, Zeng HP, Deng DJ, Xin HG, Song J, Xu CH, Sun XW, Hou XL, Wang XW, Zheng HK (2014) Construction and analysis of high-density linkage map using high-throughput sequencing data. PLoS One 9:e98855

    PubMed  PubMed Central  Google Scholar 

  • Liu CX, Li X, Meng DX, Zhong Y, Chen C, Dong X, Xu XW, Chen BJ, Li W, Li L, Tian XL, Zhao HM, Song WB, Luo HS, Zhang QH, Lai JS, Jin WW, Yan JB, Chen SJ (2017) A 4-bp insertion at ZmPLA1 encoding a putative phospholipase a generates haploid induction in maize. Mol Plant 10:520–522

    CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Mckenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M (2010) The genome analysis toolkit: a map reduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    CAS  PubMed  PubMed Central  Google Scholar 

  • McMullen MD et al (2009) Genetic properties of the maize nested association mapping population. Science 325:737–740

    CAS  PubMed  Google Scholar 

  • Mickelson SM, Stuber CS, Senior L, Kaeppler SM (2002) Quantitative trait loci controlling leaf and tassel traits in a B73× Mo17 population of maize. Crop Sci 42:1902–1909

    CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    CAS  PubMed  PubMed Central  Google Scholar 

  • Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D (2006) A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature 441:227–230

    CAS  PubMed  Google Scholar 

  • Schuetz SH, Mock JJ (1978) Genetics of tassel branch number in maize and its implications for a selection program for small tassel size. Theor Appl Genet 53:265–271

    CAS  PubMed  Google Scholar 

  • Seng TY, Ritter E, Saad SHM, Leao LJ, Singh RSH, Zaman FQ, Tan SG, Alwee SSRS, Rao V (2016) QTLs for oil yield components in an elite oil palm (Elaeis guineensis) cross. Euphytica 212:399–425

    Google Scholar 

  • Studer AJ, Wang H, Doebley JF (2017) Selection during maize domestication targeted a gene network controlling plant and inflorescence architecture. Genetics 207:755–765

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun XW, Liu DY, Zhang XF, Li WB, Liu H, Hong WG, Jiang CB, Guan N, Ma CX, Zeng HP, Xu CH, Song J, Huang L, Wang CM, Shi JJ, Wang R, Zheng XH, Lu CY, Wang XW, Zheng HK (2013) SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One 8:e58700

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang H, Yan JB, Huang YQ, Zheng YL, Li JS (2005) QTL mapping of five agronomic traits in maize. Acta Genet Sin 32:203–209

    PubMed  Google Scholar 

  • Upadyayula N, Da Silva HS, Bohn MO, Rocheford TR (2006a) Genetic and QTL analysis of maize tassel and ear inflorescence architecture. Theor Appl Genet 112:592–606

    CAS  PubMed  Google Scholar 

  • Upadyayula N, Wassom J, Bohn MO, Rocheford TR (2006b) Quantitative trait loci analysis of phenotypic traits and principal components of maize tassel inflorescence architecture. Theor Appl Genet 113:1395–1407

    CAS  PubMed  Google Scholar 

  • Vollbrecht E, Springer PS, Goh L, Buckler ES, Martienssen R (2005) Architecture of floral branch systems in maize and related grasses. Nature 436:1119–1126

    CAS  PubMed  Google Scholar 

  • Wu X, Li YX, Shi YS, Song YC, Zhang DF, Li CH, Buckler ES, Li Y, Zhang ZW, Wang TY (2016) Joint‐linkage mapping and GWAS reveal extensive genetic loci that regulate male inflorescence size in maize. Plant Biotechnol J 14:1551–1562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu GH, Wang XF, Huang C, Xu DY, Li D, Tian JG, Chen QY, Wang CL, Liang YM, Wu YY, Yang XH, Tian F (2017) Complex genetic architecture underlies maize tassel domestication. New Phytol 214:852–864

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang ZZ, Li YX, Liu C, Liu ZZ, Li CH, Li QC, Peng B, Zhang Y, Wang D, Tan WW, Sun BC, Shi YS, Song YC, Wang TY, Li Y (2012) QTL analysis of tassel-related traits in maize (Zea mays L.) using multiple connected populations. Acta Agron Sin 38:1435–1442

    CAS  Google Scholar 

  • Yang N, Lu YL, Yang XH, Huang J, Zhou Y, Ali F, Wen WW, Liu J, Li JS, Yan JB (2014) Genome wide association studies using a new nonparametric model reveal the genetic architecture of 17 agronomic traits in an enlarged maize association panel. PLoS Genet 10:e1004573

    PubMed  PubMed Central  Google Scholar 

  • Yi Q, Liu YH, Zhang XG, Hou XB, Zhang JJ, Liu HM, Hu YF, Yu GW, Huang YB (2018) Comparative mapping of quantitative trait loci for tassel-related traits of maize in F2:3 and RIL populations. J Genet 97:253–266

    CAS  PubMed  Google Scholar 

  • Zhang QX et al (2018) The genetic architecture of floral traits in the woody plant Prunus mume. Nat Commun 9:1702

    PubMed  PubMed Central  Google Scholar 

  • Zhao XQ, Peng YL, Zhang JW, Fang P, Wu BY (2017) Mapping QTLs and meta-QTLs for two inflorescence architecture traits in multiple maize populations under different watering environments. Mol Breed 37:91

    Google Scholar 

  • Zhou QH, Han DP, Mason AS, Zhou C, Zheng W, Li YZ, Wu CJ, Fu DH, Huang YJ (2017) Earliness traits in rapeseed (Brassica napus): SNP loci and candidate genes identified by genome-wide association analysis. DNA Res 25:229–244

    PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the China Department for Ministry of Science and Technology Spark Program (2015GA660007) and by the Jilin Provincial Agriculture Committee Promotion Project (ntg1807).

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Authors

Contributions

R.Z. conceived and supervised the project. Y.N.X. participated in experimental design, carried out phenotypic data analysis and drafted the manuscript. X.Y.Y. and X.C.R. prepared the experiment materials. X.Q.W. contributed to linkage map construction and QTL mapping. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Rengui Zhao.

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The authors declare that they have no competing interests.

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Communicated by: Ray Ming

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Xie, Y., Wang, X., Ren, X. et al. A SNP-Based High-Density Genetic Map Reveals Reproducible QTLs for Tassel-Related Traits in Maize (Zea mays L.). Tropical Plant Biol. 12, 244–254 (2019). https://doi.org/10.1007/s12042-019-09227-1

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