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
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
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
Brewbaker JL (2015) Diversity and genetics of tassel branch numbers in maize. Crop Sci 55:65–78
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
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
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
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
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
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
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
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
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
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
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
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
Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugenics 12:172–175
Lambert RJ, Johnson RR (1978) Leaf angle, tassel morphology, and the performance of maize hybrids. Crop Sci 18:499–502
Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754–1760
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
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
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
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
McMullen MD et al (2009) Genetic properties of the maize nested association mapping population. Science 325:737–740
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
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326
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
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
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
Studer AJ, Wang H, Doebley JF (2017) Selection during maize domestication targeted a gene network controlling plant and inflorescence architecture. Genetics 207:755–765
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
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
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
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
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
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
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
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
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
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
Zhang QX et al (2018) The genetic architecture of floral traits in the woody plant Prunus mume. Nat Commun 9:1702
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
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
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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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.
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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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DOI: https://doi.org/10.1007/s12042-019-09227-1