Log in

QTL-seq and marker development for resistance to head splitting in cabbage

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Head splitting is a major physiological disease in cabbage. The most effective approach for controlling head splitting is to deploy genetic resistance by breeding cabbage cultivars with stable resistance. However, the genetic mechanisms regulating head-splitting resistance in cabbage remain largely unknown. Here, we employed the whole-genome resequencing-based approach (QTL-seq) to discover genomic regions, candidate genes, and diagnostic markers for head-splitting resistance in an F2 segregation population derived from a cross between two inbred lines G274 (head-splitting susceptible) and G279 (head-splitting resistant). Single nucleotide polymorphism index (SNP-index) analysis indicated that one candidate genomic region spanning 5.6 Mb on chromosome 3 was responsible for head-splitting resistance. A candidate gene, Bol016058, was identified in this region, which is a homologue of proline-rich protein 4 (PRP4) and encodes a structural cell wall protein in Arabidopsis. This target gene was highly expressed in leaves, with four SNPs and one insertion-deletion (InDel) between G274 and G279. Moreover, a diagnostic InDel marker was successfully developed from this gene and validated on a set of breeding materials and could accelerate the selection of head-splitting resistant cabbage cultivars.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70:21–30

    Article  CAS  Google Scholar 

  • Branham SE, Farnham MW (2019) Identification of heat tolerance loci in broccoli through bulked segregant analysis using whole genome resequencing. Euphytica 215:34

    Article  Google Scholar 

  • Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703–1712

    Article  CAS  Google Scholar 

  • Chang BM, Keller M (2021) Cuticle and skin cell walls have common and unique roles in grape berry splitting. Hortic Res 8:168

    Article  CAS  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:i884–i890

    Article  Google Scholar 

  • Chiang MS (1972) Inheritance of head splitting in cabbage (Brassica oleracea L. var. capitata L.). Euphytica 21:507–509

    Article  Google Scholar 

  • Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms. SnpEff Fly 6:80–92

    Article  CAS  Google Scholar 

  • Fowler TJ, Bernhardt C, Tierney M (1999) Characterization and expression of four proline-rich cell wall protein genes in Arabidopsis encoding two distinct subsets of multiple domain proteins. Plant Physiol 121:1081–1091

    Article  CAS  Google Scholar 

  • Illa-Berenguer E, Van Houten J, Huang Z, van der Knaap E (2015) Rapid and reliable identification of tomato fruit weight and locule number loci by QTL-seq. Theor Appl Genet 128:1329–1342

    Article  Google Scholar 

  • Jiang F, Lopez A, Jeon S, Freitas ST, Yu Q, Wu Z, Labavitch JM, Tian S, Powell ALT, Mitcham E (2019) Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking. Hortic Res 6:17

    Article  Google Scholar 

  • Kasai S, Hayama H, Kashimura Y, Kudo S, Osanai Y (2008) Relationship between fruit cracking and expression of the expansin gene MdEXPA3 in “Fuji” apples (Malus domestica Borkh.). Sci Hortic 116:194–198

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Subgroup GPDP (2009) The Sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  Google Scholar 

  • Li Q, Shi Y, Wang Y, Liu L, Zhang X, Chen X, Zhang L, Su Y, Zhang T (2020) Breeding of cabbage lines resistant to both head splitting and fusarium wilt via an isolated microspore culture system and marker-assisted selection. Euphytica 216:34

    Article  CAS  Google Scholar 

  • Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IAP, Zhao M, Ma J, Yu J, Huang S, Wang X, Wang J, Lu K, Fang Z, Bancroft I, Yang TJ, Hu Q, Wang X, Yue Z, Li H, Yang L, Wu J, Zhou Q, Wang W, King GJ, Pires JC, Lu C, Wu Z, Sampath P, Wang Z, Guo H, Pan S, Yang L, Min J, Zhang D, ** D, Li W, Belcram H, Tu J, Guan M, Qi C, Du D, Li J, Jiang L, Batley J, Sharpe AG, Park BS, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong C, Wang L, Li J, Hu Z, Zhuang M, Huang Y, Huang J, Shi J, Mei D, Liu J, Lee TH, Wang J, ** H, Li Z, Li X, Zhang J, **ao L, Zhou Y, Liu Z, Liu X, Qin R, Tang X, Liu W, Wang Y, Zhang Y, Lee J, Kim HH, Denoeud F, Xu X, Liang X, Hua W, Wang X, Wang J, Chalhoub B, Paterson AH (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930

    Article  CAS  Google Scholar 

  • Liu T, Wang J, Wu C, Zhang Y, Zhang X, Li X, Wang H, Song J, Li X (2019) Combined QTL-Seq and traditional linkage analysis to identify candidate genes for purple skin of radish fleshy taproots. Front Genet 10:808

    Article  CAS  Google Scholar 

  • Lu H, Lin T, Klein J, Wang S, Qi J, Zhou Q, Sun J, Zhang Z, Weng Y, Huang S (2014) QTL-seq identifies an early flowering QTL located near flowering locus T in cucumber. Theor Appl Genet 127:1491–1499

    Article  Google Scholar 

  • Pang W, Li X, Choi SR, Nguyen VD, Dhandapani V, Kim YY, Ramchiary N, Kim JG, Edwards D, Batley J, Na J, Kim HR, Lim YP (2015a) Map** QTLs of resistance to head splitting in cabbage (Brassica oleracea L. var. capitata L.). Mol Breed 35:126

    Article  Google Scholar 

  • Pang W, Kim YY, Li X, Choi SR, Wang Y, Sung C, Im S, Ramchiary N, Zhou G, Lim YP (2015b) Anatomic characteristics associated with head splitting in cabbage (Brassica oleracea var. capitata L.). Plos One 10:e0142202

    Article  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shu J, Liu Y, Zhang L, Li Z, Fang Z, Yang L, Zhuang M, Zhang Y, Lv H (2018) QTL-seq for rapid identification of candidate genes for flowering time in broccoli×cabbage. Theor Appl Genet 131:917–928

    Article  CAS  Google Scholar 

  • Su Y, Liu Y, Fang Z, Yang L, Zhuang M, Zhang Y, Zhang X, Sun P (2012) Genetic analysis of head-splitting resistance traits in cabbage. Acta Hortic Sinica 39:1482–1490

    Google Scholar 

  • Su Y, Zeng A, Liu Y, Shen H, **ao X, Li Z, Fang Z, Yang L, Zhuang M, Zhang Y (2015a) Evaluation method and screening of germplasm with high resistance to head-splitting in cabbage. J Plant Genet Resour 16:1229–1236

    Google Scholar 

  • Su Y, Liu Y, Li Z, Fang Z, Yang L, Zhuang M, Zhang Y (2015b) QTL Analysis of head splitting resistance in cabbage (Brassica oleracea L. var. capitata) using SSR and InDel makers based on whole-genome re-sequencing. Plos one 10:e0138073

    Article  Google Scholar 

  • Su Y, Li Q, Yi D, Liu L, Fu C, Zhang T, Zhang H, Chen Y (2019) Genetic analysis of traits related to head in white cabbage. Northern Hortic 2019:7–14

    Google Scholar 

  • Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano LM, Kamoun S, Terauchi R (2013) QTL-seq: rapid map** of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183

    Article  CAS  Google Scholar 

  • Tan H, Wang X, Fei Z, Li H, Tadmor Y, Mazourek M, Li L (2020) Genetic map** of green curd gene Gr in cauliflower. Theor Appl Genet 133:353–364

    Article  Google Scholar 

  • Win KT, Zhang C, Silva RR, Lee HJ, Kim YC, Lee S (2019) Identification of quantitative trait loci governing subgynoecy in cucumber. Theor Appl Genet 132:1505–1521

    Article  CAS  Google Scholar 

  • Yan C, Huang Y, Liu Z, Guo F, Jiao Z, Yang W, Zhu F, Qiu Z (2020) Rapid identification of yellow-flowered gene Bofc in cauliflower (Brassica oleracea var. botrytis) by bulked segregant analysis and whole-genome resequencing. Euphytica 216:26

    Article  CAS  Google Scholar 

  • Yong W, Lu W, Li J, Jiang Y (2006) Differential expression of two expansin genes in develo** fruit of cracking-susceptible and -resistant litchi cultivars. J Am Soc Hortic Sci 1:118–121

    Article  Google Scholar 

  • Zeng A, Liu Y, Fang Z, Yan J (2011) Research progress of head splitting on cabbage (Brassica oleracea L. var. capitata L.). J Plant Genet Resour 12:307–310

    CAS  Google Scholar 

  • Zeng A, Liu Y, Fang Z, Yang L, Zhuang M, Zhang Y, Sun P (2009) Studies on relationship between splitting tolerant characteristics and surface micro-configuration and cell tissue structure of leaf in cabbage (Brassica oleracea L. var. capitata L.). Acta Agric Boreali-Sinca 24:41–45

    CAS  Google Scholar 

  • Zhuang M, Zhang Y, Fang Z, Liu Y, Yang L, Sun P (2009) Studies on combining ability and heritability of splitting-resistance characteristic in cabbage (Brassica oleracea var. capitata L.). China Veg 2009:12–15

    Google Scholar 

Download references

Funding

This research was funded by the Agricultural Development Program through Science and Technology of Shanghai (2022-02-08-00-12-F01099), the Agricultural Field Project of Shanghai Science and Technology Innovation Action Plan (21N51900400), the China Agriculture Research System (Grant No. CARS-25).

Author information

Authors and Affiliations

Authors

Contributions

XZ conceptualised and designed the experiments and wrote the manuscript; XZ, XT, YR, MW, JC, and TB performed the experiments and analysed the data.

Corresponding authors

Correspondence to **xiu Chen or Tianyue Bo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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.

Online resource 1

Candidate genes based on functional annotation of the SNPs with a minimum read depth of 10, and an SNP-index near 1 (≥ 0.7) and 0 (≤ 0.3) in R-bulk and S-bulk, respectively. Online resource 2 Genomic DNA sequences alignment of the Bol016058 in G274 and G279. Online resource 3 Genotypes of the diagnostic marker in inbred lines with different resistances to head splitting.Online resource 4 Primers used in this study (RAR 45 kb)

Supplementary file2 (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhu, X., Tai, X., Ren, Y. et al. QTL-seq and marker development for resistance to head splitting in cabbage. Euphytica 218, 41 (2022). https://doi.org/10.1007/s10681-022-02982-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-022-02982-5

Keywords

Navigation