Skip to main content
Log in

Both overlapping and independent loci underlie seed number per pod and seed weight in Brassica napus by comparative quantitative trait loci analysis

  • Published:
Molecular Breeding Aims and scope Submit manuscript

A Correction to this article was published on 27 August 2021

This article has been updated

Abstract

Seed number per pod (SNPP) and seed weight (SW) are two components of seed yield in rapeseed (Brassica napus). Here, a natural population of rapeseed was employed for genome-wide association analysis for SNPP and SW across multi-years. A total of 101 and 77 SNPs significantly associated with SNPP and SW with the phenotypic variances (R2) ranging from 1.35 to 29.47% and from 0.78 to 34.58%, respectively. And 43 and 33 homologs of known genes from model plants were located in the 65 and 49 haplotype blocks (HBs) for SNPP and SW, respectively. Notably, we found 5 overlapping loci and 3 sets of loci with collinearity for both SNPP and SW, of which 4 overlapping loci harbored the haplotypes with the same direction of genetic effects on SNPP and SW, indicating high possibility to simultaneously improve SNPP and SW in rapeseed. Our findings revealed both overlapping and independent loci controlling seed number per pod and seed weight in rapeseed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

The data sets supporting the results of this article are included within the article and its additional files.

Code availability

The code and materials analyzed during the current study are available from the corresponding author on reasonable request.

Change history

References

  • Bahaji A, Almagro G, Ezquer I, Gámez-Arcas S, Sánchez-López ÁM, Muñoz FJ, Barrio RJ, Sampedro MS, Diego ND, Spíchal L, Doležal K, Tarkowská D, Caporali E, Mendes MA, Baroja-Fernández E, Pozueta-Romero J (2018) Plastidial phosphoglucose isomerase is an important determinant of seed yield through its involvement in gibberellin-mediated reproductive development and storage reserve biosynthesis in Arabidopsis. Plant Cell 30(9):2082–2098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basunanda P, Radoev M, Ecke W, Friedt W, Becker HC, Snowdon RJ (2010) Comparative mapping of quantitative trait loci involved in heterosis for seedling and yield traits in oilseed rape (Brassica napus L.). Theor Appl Genet 120(2):271–281

    Article  CAS  PubMed  Google Scholar 

  • Bayer PE, Hurgobin B, Golicz AA, Chan CKK, Yuan YX, Lee HT, Renton M, Meng JL, Li RY, Long Y, Zou J, Bancroft I, Chalhoub B, King GJ, Batley J, Edwards D (2017) Assembly and comparison of two closely related Brassica napus genomes. Plant Biotechnol J 15(12):1602–1610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai DF, Xiao YJ, Yang W, Ye W, Wang B, Younas M, Wu JS, Liu KD (2014) Association mapping of six yield-related traits in rapeseed (Brassica napus L.). Theor Appl Genet 127(1):85–96

    Article  CAS  PubMed  Google Scholar 

  • Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang HB, Wang XY, Chiquet J, Belcram H, Tong CB, Samans B, Corréa M, Silva CD, Just J, Falentin C, Koh CS, Clainche IL, Bernard M, Bento P, Noel B, Labadie K et al (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Sci 345(6199):950–953

    Article  CAS  Google Scholar 

  • Chen W, Zhang YS, Yao JB, Ma CZ, Tu JX, Fu TD (2011) Quantitative trait loci mapping for two seed yield component traits in an oilseed rape (Brassica napus) cross. Plant Breeding 130:640–646

    Article  Google Scholar 

  • Ding GD, Zhao ZK, Liao Y, Hu YF, Shi L, Long Y, Xu FS (2012) Quantitative trait loci for seed yield and yield-related traits, and their responses to reduced phosphorus supply in Brassica napus. Ann Bot 109(4):747–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong HL, Tan CD, Li YZ, He Y, Wei S, Cui YX, Chen YG, Wei DY, Fu Y, He YJ, Wan HY, Liu Z, Xiong Q, Lu K, Li JN, Qian W (2018) Genome-wide association study reveals both overlapping and independent genetic loci to control seed weight and silique length in Brassica napus. Front Plant Sci 9:921

    Article  PubMed  PubMed Central  Google Scholar 

  • Fan CC, Cai GQ, Qin J, Li QY, Yang MY, Wu JZ, Fu TD, Liu KD, Zhou YM (2010) Mapping of quantitative trait loci and development of allele-specific markers for seed weight in Brassica napus. Theor Appl Genet 121(7):1289–1301

    Article  CAS  PubMed  Google Scholar 

  • Freund RJ, Littell RC (1981) SAS for linear models: a guide to the ANOVA and GLM procedures. SAS Institute Inc, Cary (SAS users guide: Basics)

    Google Scholar 

  • Fu Y, Wei DY, Dong HL, He YJ, Cui YX, Mei JQ, Wan HF, Li JN, Snowdon R, Friedt W, Li XR, Qian W (2015) Comparative quantitative trait loci for silique length and seed weight in Brassica napus. Sci Rep 5:14407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge Z, Cheung AY, Qu LJ (2019) Pollen tube integrity regulation in flowering plants: insights from molecular assemblies on the pollen tube surface. New Phytol 222(2):687–693

    Article  PubMed  Google Scholar 

  • Guo T, Chen K, Dong NQ, Shi CL, Ye WW, Gao JP, Shan JX, Lin HX (2018) GRAIN SIZE AND NUMBER1 negatively regulates the OsMKKK10-OsMKK4-OsMPK6 cascade to coordinate the trade-off between grain number per panicle and grain size in Rice. Plant Cell 30(4):871–888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua W, Li RJ, Zhan GM, Liu J, Li J, Wang XF, Liu GH, Wang HZ (2012) Maternal control of seed oil content in Brassica napus: the role of silique wall photosynthesis. Plant J 69(3):432–444

    Article  CAS  PubMed  Google Scholar 

  • Kowles R (2001) Solving Problems in Genetics. Springer-Verlag, New York

    Book  Google Scholar 

  • Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamprianou I (2013) Application of single-level and multi-level Rasch models using the lme4 package. J Appl Meas 14(1):79–90

  • Li N, Shi JQ, Wang XF, Liu GH, Wang HZ (2014) A combined linkage and regional association mapping validation and fine mapping of two major pleiotropic QTLs for seed weight and silique length in rapeseed (Brassica napus L.). BMC Plant Biol 14:114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li N, Xu R, Li Y (2019) Molecular networks of seed size control in plants. Annu Rev Plant Biol 70:435–463

    Article  CAS  PubMed  Google Scholar 

  • Li SP, Chen L, Zhang LW, Li X, Liu Y, Wu ZK, Dong FM, Wan LL, Liu KD, Hong DF, Yang GS (2015) BnaC9. SMG7b functions as a positive regulator of the number of seeds per silique in Brassica napus by regulating the formation of functional female gametophytes. Plant Physiol 169(4):2744–2760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu SY, Liu YM, Yang XH, Tong CB, Edwards D, Parkin IAP, Zhao MX, Ma JX, Yu JY, Huang SM, Wang XY, Wang JY, Lu K, Fang ZY, Bancroft I, Yang TJ, Hu Q, Wang XF, Yue Z, Li HJ et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Hua W, Hu ZY, Yang HL, Zhang L, Li RJ, Deng LB, Sun XC, Wang XF, Wang HZ (2015) Natural variation in ARF18 gene simultaneously affects seed weight and silique length in polyploid rapeseed. Proc Natl Acad Sci USA 112(37):E5123–E5132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu GY, Zhang F, Zheng PY, Cheng Y, Liu FL, Fu GP, Zhang XK (2011) Relationship among yield components and selection criteria for yield improvement in early rapeseed (Brassica napus L.). Agricultural Sci in China 10(7):997–1003

    Article  Google Scholar 

  • Lu K, Peng L, Zhang C, Lu JH, Yang B, Xiao ZC, Liang Y, Xu XF, Qu CM, Zhang K, Liu LZ, Zhu QL, Fu ML, Yuan XY, Li JN (2017) Genome-wide association and transcriptome analyses reveal candidate genes underlying yield-determining traits in Brassica napus. Front Plant Sci 8:206

    PubMed  PubMed Central  Google Scholar 

  • Luo ZL, Wang M, Long Y, Huang YJ, Shi L, Zhang CY, Liu X, Fitt BDL, Xiang JX, Mason AS, Snowdon RJ, Liu PF, Meng JL, Zou J (2017) Incorporating pleiotropic quantitative trait loci in dissection of complex traits: seed yield in rapeseed as an example. Theor Appl Genet 130(8):1569–1585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller C, Wells R, McKenzie N, Trick M, Ball J, Fatihi A, Dubreucq B, Chardot T, Lepiniec L, Bevan MW (2019) Variation in expression of the HECT E3 ligase UPL3 modulates LEC2 levels, seed size, and crop yields in Brassica napus. Plant Cell 31(10):2370–2385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi LP, Mao L, Sun CM, Pu YY, Fu TD, Ma CZ, Shen JX, Tu JX, Yi B, Wen J (2014) Interpreting the genetic basis of silique traits in Brassica napus using a joint QTL network. Plant Breeding 133:52–60

    Article  CAS  Google Scholar 

  • Qian L, Qian W, Snowdon RJ (2016) Haplotype hitchhiking promotes trait coselection in Brassica napus. Plant Biotechnol J 14(7):1578–1588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu LJ, Li L, Lan Z, Dresselhaus T (2015) Peptide signalling during the pollen tube journey and double fertilization. J Exp Bot 66(17):5139–5150

    Article  CAS  PubMed  Google Scholar 

  • Quijada PA, Udall JA, Lambert B, Osborn TC (2006) Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed (Brassica napus L.): 1. Identification of genomic regions from winter germplasm. Theor Appl Genet 113(3):549–561

    Article  CAS  PubMed  Google Scholar 

  • Radoev M, Becker HC, Ecke W (2008) Genetic analysis of heterosis for yield and yield components in rapeseed (Brassica napus L.) by quantitative trait locus mapping. Genetics 179(3):1547–1558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raman H, Raman R, Coombes N, Song J, Prangnell R, Bandaranayake C, Tahira R, Sundaramoorthi V, Killian A, Meng J, Dennis ES, Balasubramanian S (2016) Genome-wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola. Plant Cell Environ 39(6):1228–1239

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Hernández AA, Muro-Medina CV, Ramírez-Alonso JI, Jiménez-Bremont JF (2017) Modification of AtGRDP1 gene expression affects silique and seed development in Arabidopsis thaliana. Biochem Biophys Res Commun 486(2):252–256

    Article  PubMed  CAS  Google Scholar 

  • Shahid M, Cai GQ, Zu F, Zhao Q, Qasim MU, Hong YY, Fan CC, Zhou YM (2019) Comparative transcriptome analysis of developing seeds and silique wall reveals dynamic transcription networks for effective oil production in Brassica napus L. Int J Mol Sci 20(8):1982

    Article  CAS  PubMed Central  Google Scholar 

  • Shi JQ, Li RY, Qiu D, Jiang CC, Long Y, Morgan C, Bancroft I, Zhao JY, Meng JL (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182(3):851–861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi JQ, Li RY, Zou J, Long Y, Meng JL (2011) A dynamic and complex network regulates the heterosis of yield-correlated traits in rapeseed (Brassica napus L.). PLoS One 6(7):e21645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi JQ, Zhan JP, Yang YH, Ye J, Huang SM, Li RY, Wang XF, Liu GH, Wang HZ (2015) Linkage and regional association analysis reveal two new tightly-linked major-QTLs for pod number and seed number per pod in rapeseed (Brassica napus L.). Sci Rep 5:14481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi LL, Song JR, Guo CC, Wang B, Guan ZL, Yang P, Chen X, Zhang QH, King GJ, Wang J, Liu KD (2019) A CACTA-like transposable element in the upstream region of BnaA9.CYP78A9 acts as an enhancer to increase silique length and seed weight in rapeseed. Plant J 98(3):524–539

    Article  CAS  PubMed  Google Scholar 

  • Shin HY, Nam KH (2018) RAV1 negatively regulates seed development by directly repressing MINI3 and IKU2 in Arabidopsis. Mol Cells 41(12):1072–1080

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shin JH, Blay S, Mcneney B, Graham J (2006) LDheatmap: An R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. J Stat Soft 16:1–9

    Article  Google Scholar 

  • Soderlund C, Bomhoff M, Nelson WM (2011) SyMAP v3.4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res 39(10):e68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song JM, Guan ZL, Hu JL, Guo CC, Yang ZQ, Wang S, Liu DX, Wang B, Lu SP, Zhou R, Xie WZ, Cheng YF, Zhang YT, Liu KD, Yang QY, Chen LL, Guo L (2020) Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nat Plants 6(1):34–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun FM, Fan GY, Hu Q, Zhou YM, Guan M, Tong CB, Li JN, Du DZ, Qi CK, Jiang LC, Liu WQ, Huang SM, Chen WB, Yu JY, Mei DS, Meng JL, Zeng P, Shi JQ, Liu KD, Wang X (2017) The high-quality genome of Brassica napus cultivar ‘ZS11’ reveals the introgression history in semi-winter morphotype. Plant J 92(3):452–468

    Article  CAS  PubMed  Google Scholar 

  • Turner SD (2014) qqman: An R package for visualizing GWAS results using QQ and manhattan plots. BioRxiv. https://doi.org/10.1101/005165

    Article  Google Scholar 

  • UN (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jap J Bot 7:389–452

    Google Scholar 

  • Udall JA, Quijada PA, Lambert B, Osborn TC (2006) Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed (Brassica napus L.): 2. Identification of alleles from unadapted germplasm. Theor Appl Genet 113(4):597–609

    Article  CAS  PubMed  Google Scholar 

  • Wagner GP, Zhang JZ (2011) The pleiotropic structure of the genotype-phenotype map: the evolvability of complex organisms. Nat Rev Genet 12(3):204–213

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Guan CY (2010) Molecular mapping and identification of quantitative trait loci for yield components in rapeseed (Brasscia napus L.). Hereditas 32(3):271–277

    CAS  PubMed  Google Scholar 

  • Wang JL, Tang MQ, Chen S, Zheng XF, Mo HX, Li SJ, Wang Z, Zhu KM, Ding LN, Liu SY, Li YH, Tan XL (2017a) Down-regulation of BnDA1, whose gene locus is associated with the seeds weight, improves the seeds weight and organ size in Brassica napus. Plant Biotechnol J 15(8):1024–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang ML, Lu XD, Xu GY, Yin XM, Cui YC, Huang LF, Rocha PSCF, Xia XJ (2016a) OsSGL, a novel pleiotropic stress-related gene enhances grain length and yield in rice. Sci Rep 6:38157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SS, Wu K, Qian Q, Liu Q, Li Q, Pan YJ, Ye YF, Liu XY, Wang J, Zhang JQ, Li S, Wu YJ, Fu XD (2017b) Non-canonical regulation of SPL transcription factors by a human OTUB1-like deubiquitinase defines a new plant type rice associated with higher grain yield. Cell Res 27(9):1142–1156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XW, Wang HZ, Wang J, Sun RF, Wu J, Liu SY, Bai YQ, Mun JH, Bancroft I, Cheng F, Huang SW, Li XX, Hua W, Wang JY, Wang XY, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43(10):1035–1039

    Article  CAS  PubMed  Google Scholar 

  • Wang XD, Chen L, Wang AN, Wang H, Tian JH, Zhao XP, Chao HB, Zhao YJ, Zhao WG, Xiang J, Gan JP, Li MT (2016b) Quantitative trait loci analysis and genome-wide comparison for silique related traits in Brassica napus. BMC Plant Biol 16:71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang P, Shu C, Chen L, Xu JS, Wu JS, Liu KD (2012) Identification of a major QTL for silique length and seed weight in oilseed rape (Brassica napus L.). Theor Appl Genet 125(2):285–296

    Article  PubMed  Google Scholar 

  • Yang YH, Shi JQ, Wang XF, Liu GH, Wang HZ (2016) Genetic architecture and mechanism of seed number per pod in rapeseed: elucidated through linkage and near-isogenic line analysis. Sci Rep 6:24124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Shen YS, Li SD, Ge XH, Li ZY (2017) High density linkage map construction and QTL detection for three silique-related traits in Orychophragmus violaceus derived Brassica napus population. Front Plant Sci 8:1512

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Zhu KY, Li HL, Han SQ, Meng QW, Khan SU, Fan CC, Xie KB, Zhou YM (2018) Precise editing of CLAVATA genes in Brassica napus L. regulates multilocular silique development. Plant Biotechnol J 16(7):1322–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan H, Qin P, Hu L, Zhan SJ, Wang SF, Gao P, Li J, Jin MY, Xu ZY, Gao Q, Du AP, Tu B, Chen WL, Ma BT, Wang YP, Li SG (2019) OsSPL18 controls grain weight and grain number in rice. J Genet Genomics 46(1):41–51

    Article  PubMed  Google Scholar 

  • Zhang LW, Liu PW, Hong DF, Huang AQ, Li SP, He QB, Yang GS (2010) Inheritance of seeds per silique in Brassica napus L. using joint segregation analysis. Field Crop Res 116:58–67

    Article  Google Scholar 

  • Zhang LW, Yang GS, Liu PW, Hong DF, Li SP, He QB (2011) Genetic and correlation analysis of silique-traits in Brassica napus L. by quantitative trait locus mapping. Theor Appl Genet 122(1):21–31

    Article  PubMed  Google Scholar 

  • Zhang SF, Fu TD, Zhu JC, Wang JP, Wen YC, Ma CZ (2006) QTL mapping and epistasis analysis for yield and its components in Brassica napus L. Acta Agron Sin 32:1135–1142

    CAS  Google Scholar 

  • Zhang YW, Tamba CL, Wen YJ, Li P, Ren WL, Ni YL, Gao J, Zhang YM (2020) mrMLM v4.0: An R platform for multi-locus genome-wide association studies. Genomics Proteomics Bioinformatics. https://doi.org/10.1016/j.gpb.2020.06.006

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao MZ, Zhao MH, Gu S, Sun J, Ma ZB, Wang LL, Zheng WJ, Xu ZJ (2019) DEP1 is involved in regulating the carbon-nitrogen metabolic balance to affect grain yield and quality in rice (Oriza sativa L.). PLoS One 14(3):e0213504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu XY, Zhang L, Kuang C, Guo Y, Huang CQ, Deng LB, Sun XC, Zhan GM, Hu ZY, Wang HZ, Hua W (2018) Important photosynthetic contribution of silique wall to seed yield-related traits in Arabidopsis thaliana. Photosynth Res 137(3):493–501

    Article  CAS  PubMed  Google Scholar 

  • Zhu YY, Ye J, Zhan JP, Zheng XX, Zhang JJ, Shi JQ, Wang XF, Liu GH, Wang HZ (2020) Validation and characterization of a seed number per silique quantitative trait locus qSN A7 in rapeseed (Brassica napus L.). Front Plant Sci 11:68

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study was funded by National Key Research and Development Program (2016YFD0100202), National Program on Key Basic Research Project of China (2015CB150201), National Nature Science Foundation of China (31471529), and the Project of Chongqing Science and Technology Commission (cstc2019jcyj-zdxmX0012, XmT2018081, and cstc2019jcyj-bshX0055).

Author information

Authors and Affiliations

Authors

Contributions

WQ, SX, and HD conceived and designed the study. SX, HD, LY, DH, FZ, YC, SW, and JL participated in the phenotyping of seed number per pod and seed weight and performed the experiments. SX, HD, YH, HW, ZL, and XL contributed to data analysis and interpretation. SX, HD, and WQ wrote the paper. All authors reviewed the manuscript.

Corresponding author

Correspondence to Wei Qian.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 21175 KB)

Supplementary file2 (XLSX 93 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xin, S., Dong, H., Yang, L. et al. Both overlapping and independent loci underlie seed number per pod and seed weight in Brassica napus by comparative quantitative trait loci analysis. Mol Breeding 41, 41 (2021). https://doi.org/10.1007/s11032-021-01232-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-021-01232-1

Keywords

Navigation