Skip to main content
Log in

Role of BrSDG8 on bolting in Chinese cabbage (Brassica rapa)

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Mapping and resequencing of two allelic early bolting mutants ebm5-1 and ebm5-2 revealed that the BrSDG8 gene is related to bolting in Chinese cabbage (Brassica rapa ssp. pekinensis).

Abstract

Bolting influences the leafy head formation and seed yield of Chinese cabbage therefore being an important agronomic trait. Herein, two allelic early bolting mutants, ebm5-1 and ebm5-2, stably inherited in Chinese cabbage were obtained from wild-type ‘FT’ seeds by ethyl methane sulfonate mutagenesis. Both mutants flowered significantly earlier than ‘FT,’ and genetic analysis revealed that the early bolting of the two mutants was controlled by one recessive nuclear gene. With BSR-seq, the mutations originating lines ebm5-1 and ebm5-2 were located to the same region in chromosome A07. Using the 1741 F2 individuals with the ebm5-1 phenotype as the mapping population, this region was narrowed to 56.24 kb between markers InDel18 and InDel45. A single-nucleotide polymorphism (SNP) was aligned to the BraA07g040740.3C (BrSDG8) region by whole-genome resequencing of ebm5-1 mutant and ‘FT.’ BrSDG8 is a homolog of Arabidopsis thaliana SDG8 encoding a histone methyltransferase affecting H3K4 trimethylation in FLOWERING LOCUS C chromatin. Comparative sequencing established that the SNP occurred on BrSDG8 17th exon in ebm5-1. Genotype analysis showed full co-segregation of the early bolting phenotype with this SNP. Cloning of allelic mutant ebm5-2 indicated that it harbors a deletion mutation on the 12th exon of BrSDG8. Quantitative real-time PCR analysis indicated that BrSDG8 expression level was observably lower in mutant ebm5-1 than in ‘FT.’ Overall, the present results provide strong evidence that BrSDG8 mutation leads to early bolting in Chinese cabbage, thereby providing a basis to understand the molecular mechanisms underlying this phenotype.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alexandre CM, Hennig L (2008) FLC or not FLC: the other side of vernalization. J Exp Bot 59(6):1127–1135

    CAS  PubMed  Google Scholar 

  • Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125(4):655–664

    PubMed  Google Scholar 

  • Behm-Ansmant I, Izaurralde E (2006) Quality control of gene expression: a stepwise assembly pathway for the surveillance complex that triggers nonsense-mediated mRNA decay. Genes Dev 20(4):391–398

    CAS  PubMed  Google Scholar 

  • Berr A, Shafiq S, Shen WH (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809(10):567–576

    CAS  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30(15):2114–2120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16(Suppl):S18–S31

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brogna S, Wen J (2009) Nonsense-mediated mRNA decay (NMD) mechanisms. Nat Struct Mol Biol 16(2):107–113

    CAS  PubMed  Google Scholar 

  • Dillon SC, Zhang X, Trievel RC, Cheng X (2005) The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 6(8):227

    PubMed  PubMed Central  Google Scholar 

  • He Y, Amasino RM (2005) Role of chromatin modification in flowering-time control. Trends Plant Sci 10(1):30–35

    CAS  PubMed  Google Scholar 

  • He Y, Doyle MR, Amasino RM (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18(22):2774–2784

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Liu C, Shen WH, Ying R (2011) Phylogenetic analysis and classification of the Brassica rapa SET-domain protein family. BMC Plant Biol 11:175

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huang SN, Liu ZY, Yao RP, Li DY, Feng H (2015) Comparative transcriptome analysis of the petal degeneration mutant pdm in Chinese cabbage (Brassica campestris ssp. pekinensis) using RNA-seq. Mol Genet Genomics 290(5):1833–1847

    CAS  PubMed  Google Scholar 

  • Huang SN, Liu ZY, Yao RP et al (2016) Candidate gene prediction for a petal degeneration mutant, pdm, of the Chinese cabbage (Brassica campestris ssp. pekinensis) by using fine mapping and transcriptome analysis. Mol Breed 36(3):26

    CAS  Google Scholar 

  • Huo H, Henry IM, Coppoolse ER, Verhoef-Post M, Schut JW, de Rooij H, Vogelaar A, Joosen RV, Woudenberg L, Comai L, Bradford KJ (2016) Rapid identification of lettuce seed germination mutants by bulked segregant analysis and whole genome sequencing. Plant J 88(3):345–360

    CAS  PubMed  Google Scholar 

  • Jack T (2004) Molecular and genetic mechanisms of floral control. Plant Cell 16(Suppl):S1–S17

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang D, Yang W, He Y, Amasino RM (2007) Arabidopsis relatives of the human lysine-specific demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19(10):2975–2987

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang D, Wang Y, Wang Y, He Y (2008) Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS ONE 3(10):e3404

    PubMed  PubMed Central  Google Scholar 

  • Jiang L, Li D, Jin L, Ruan Y, Shen WH, Liu C (2018) Histone lysine methyltransferases BnaSDG8.A and BnaSDG8.C are involved in the floral transition in Brassica napus. Plant J 95:672–685

    CAS  Google Scholar 

  • Jiao Y, Burow G, Gladman N, Acosta-Martinez V, Chen J, Burke J, Ware D, Xin Z (2017) Efficient identification of causal mutations through sequencing of bulked F 2 from two allelic bloomless mutants of sorghum bicolor. Front Plant Sci 8:2267

    PubMed  Google Scholar 

  • Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290(5490):344–347

    CAS  PubMed  Google Scholar 

  • Kim SY, Michaels SD (2006) SUPPRESSOR OF FRI 4 encodes a nuclear-localized protein that is required for delayed flowering in winter-annual Arabidopsis. Development 133(23):4699–4707

    CAS  PubMed  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61(9):2247–2254

    CAS  PubMed  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14):1754–1760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25(16):2078–2079

    PubMed  PubMed Central  Google Scholar 

  • Liu F, Quesada V, Crevillén P, Bäurle I, Swiezewski S, Dean C (2007) The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28(3):398–407

    PubMed  Google Scholar 

  • Liu B, Berr A, Chang C, Liu C, Shen WH, Ruan Y (2016a) Interplay of the histone methyltransferases SDG8 and SDG26 in the regulation of transcription and plant flowering and development. Biochim Biophys Acta 1859(4):581–590

    CAS  PubMed  Google Scholar 

  • Liu YT, Li CY, Shi XX, Feng H, Wang YG (2016b) Identification of QTLs with additive, epistatic, and QTL x environment interaction effects for the bolting trait in Brassica rapa L. Euphytica 210:427–439

    CAS  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 

  • Maple J, Møller SG (2007) Mutagenesis in Arabidopsis. Methods Mol Biol 362:197–206

  • McKenna A, Hanna M, Banks E et al (2010) The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303

    CAS  PubMed  PubMed Central  Google Scholar 

  • Michaels SD (2004) Flowering time regulation produces much fruit. Curr Opin Plant Biol 12(1):75–80

    Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11(5):949–956

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14(Suppl):S111–S130

    CAS  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8(19):4321–4325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Niu L, Lu F, Pei Y, Liu C, Cao X (2007) Regulation of flowering time by the protein arginine methyltransferase AtPRMT10. EMBO Rep 8(12):1190–1195

    CAS  PubMed  PubMed Central  Google Scholar 

  • Niu L, Zhang Y, Pei Y, Liu C, Cao X (2008) Redundant requirement for a pair of PROTEIN ARGININE METHYLTRANSFERASE4 homologs for the proper regulation of Arabidopsis flowering time. Plant Physiol 148(1):490–503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nordström KJ, Albani MC, James GV, Gutjahr C, Hartwig B, Turck F, Paszkowski U, Coupland G, Schneeberger K (2013) Mutation identification by direct comparison of whole-genome sequencing data from mutant and wild-type individuals using k-mers. Nat Biotechnol 31(4):325–330

    PubMed  Google Scholar 

  • Pien S, Fleury D, Mylne JS, Crevillen P, Inzé D, Avramova Z, Dean C, Grossniklaus U (2008) ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20(3):580–588

    CAS  PubMed  PubMed Central  Google Scholar 

  • Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. BioEssays 26(4):363–373

    CAS  PubMed  Google Scholar 

  • Schmitz RJ, Amasino RM (2007) Vernalization: a model for investigating epigenetics and eukaryotic gene regulation in plants. Biochim Biophys Acta 1769(5–6):269–275

    CAS  PubMed  Google Scholar 

  • Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97(7):3753–3758

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simpson GG, Gendall AR, Dean C (1999) When to switch to flowering. Annu Rev Cell Dev Biol 15:519–550

    CAS  PubMed  Google Scholar 

  • Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464

    CAS  PubMed  Google Scholar 

  • Springer NM, Kaeppler SM (2003) Comparative analysis of SET domain proteins in Maize and Arabidopsis reveals multiple duplications preceding the divergence of monocots and dicots. Plant Physiol 132(2):907–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Strahl BD, Grant PA, Briggs SD, Sun ZW, Bone JR, Caldwell JA, Mollah S, Cook RG, Shabanowitz J, Hunt DF, Allis CD (2002) Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol 22(5):1298–1306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Su A, Song W, Xing J, Zhao Y, Zhang R, Li C, Duan M, Luo M, Shi Z, Zhao J (2016) Identification of genes potentially associated with the fertility instability of S-type cytoplasmic male sterility in maize via bulked segregant RNA-Seq. PLoS ONE 11(9):e0163489

    PubMed  PubMed Central  Google Scholar 

  • Tan C, Liu ZY, Huang SN, Feng H (2018) Mapping of the male sterile mutant gene ftms in Brassica rapa L. ssp. pekinensis via BSR-Seq combined with whole–genome resequencing. Theor Appl Genet 132:355–370

    PubMed  Google Scholar 

  • Tang X, Wang Y, Zhang Y, Huang S, Liu Z, Fei D, Feng H (2018) A missense mutation of plastid RPS4 is associated with chlorophyll deficiency in Chinese cabbage (Brassica campestris ssp. pekinensis). BMC Plant Biol 18(1):130

    PubMed  PubMed Central  Google Scholar 

  • Van Ooijen J (2006) Joinmap 4.0 software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Cambridge

    Google Scholar 

  • Wang X, Zhang Y, Ma Q, Zhang Z, Xue Y, Bao S, Chong K (2007) SKB1-mediated symmetric dimethylation of histone H4R3 controls flowering time in Arabidopsis. EMBO J 26(7):1934–1941

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38(16):e164

    PubMed  PubMed Central  Google Scholar 

  • Wang N, Liu ZY, Zhang Y, Li CY, Feng H (2018) Identification and fine mapping of a stay-green gene (Brnye1) in pakchoi (Brassica campestris L. ssp. chinensis). Theor Appl Genet 131(3):673–684

    CAS  PubMed  Google Scholar 

  • Xu L, Zhao Z, Dong A, Soubigou-Taconnat L, Renou JP, Steinmetz A, Shen WH (2008) Di- and tri- but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol Cell Biol 28(4):1348–1360

    CAS  PubMed  Google Scholar 

  • Yang X, Yu Y, Zhang F, Zou Z, Zhao X, Zhang D, Xu J (2007) Linkage map construction and quantitative trait loci analysis for bolting based on a double haploid population of Brassica rapa. J Integr Plant Biol 49(5):664–671

    CAS  Google Scholar 

  • Zhang X (2012) In: Wendel J, Greilhuber J, Dolezel J, Leitch I (eds) Plant genome diversity, vol 1. Springer, Vienna, pp 237–255

    Google Scholar 

  • Zhao Z, Yu Y, Meyer D, Wu C, Shen WH (2005) Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3K36. Nat Cell Biol 7(12):1256–1260

    PubMed  Google Scholar 

Download references

Acknowledgements

The research was supported by the National Natural Science Foundation of China (Grant No. 31730082). We would like to thank Editage for English language editing.

Author information

Authors and Affiliations

Authors

Contributions

WF and SH have equally contributed to this work. HF and ZL designed the experiments. YG, MZ, and GQ helped developing the mutants. WF conducted the experiments and wrote the manuscript. WF and NW performed the data analysis. HF and SH revised the manuscript. All authors reviewed and approved this submission. The authors note that this research was performed and reported in accordance with ethical standards of the scientific conduct.

Corresponding authors

Correspondence to Zhiyong Liu or Hui Feng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

The authors note that this research was performed and reported in accordance with ethical standards of the scientific conduct.

Additional information

Communicated by Maria Laura Federico.

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 613 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fu, W., Huang, S., Gao, Y. et al. Role of BrSDG8 on bolting in Chinese cabbage (Brassica rapa). Theor Appl Genet 133, 2937–2948 (2020). https://doi.org/10.1007/s00122-020-03647-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-020-03647-4

Navigation