Skip to main content
SpringerLink
Log in

Fine mapping and candidate gene identification of the genic male-sterile gene ms3 in cabbage 51S

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

Abstract

Key message

The ms3 gene responsible for a male-sterile phenotype in cabbage was mapped to a 187.4-kb genomic fragment. The gene BoTPD1, a homolog of Arabidopsis TPD1, was identified as a strong candidate gene.

Abstract

Cabbage 51S is a spontaneous male-sterile mutant. Phenotypic investigation revealed defects in anther cell differentiation, with failure to form the tapetum layer and complete abortion of microsporocytes before the tetrad stage. Genetic analysis indicated that this male sterility was controlled by a single recessive gene, ms3. Using an F2 population, we mapped ms3 to a 187.4-kb interval. BoTPD1 was identified as a candidate from this interval. Sequence analysis revealed an intronic 182-bp insertion in 51S that interrupted the conserved motif at the 5′ splicing site of the third intron, possibly resulting in a truncated transcript. Analyses of BoTPD1 homologous proteins revealed evolutionarily conserved roles in anther cell fate determination during reproductive development. RT-PCR showed that BoTPD1 was expressed in various tissues, excluding the root, and high expression levels were detected in anthers and buds. A BoTPD1-specific marker based on the 182-bp insertion cosegregated with male sterility and can be used for marker-assisted selection.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abe Y, Mieda K, Ando T, Kono I, Yano M, Kitano H, Iwasaki Y (2010) The SMALL AND ROUND SEED1 (SRS1/DEP2) gene is involved in the regulation of seed size in rice. Genes Genet Syst 85:327–339

    Article  CAS  Google Scholar 

  • Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13:1803–1818

    Article  CAS  Google Scholar 

  • Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 174(3):483–498

    Article  CAS  Google Scholar 

  • Carmel I, Tal S, Vig I, Ast G (2004) Comparative analysis detects dependencies among the 5′ splice-site positions. RNA 10:828–840

    Article  CAS  Google Scholar 

  • Chang Z, Chen Z, Wang N, Xie G, Lu J, Yan W, Zhou J, Tang X, Deng XW (2016) Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene. Proc Natl Acad Sci 113:14145–14150

    Article  CAS  Google Scholar 

  • Chen L, Liu Y (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    Article  CAS  Google Scholar 

  • Fang Z, Sun P, Liu Y, Yang L, Wang X, Hou A, Bian C (1997) A male sterile line with dominant gene (Ms) in cabbage (Brassica oleracea var. capitata) and its utilization for hybrid seed production. Euphytica 97:265–268

    Article  Google Scholar 

  • Feng X, Dickinson HG (2010) Tapetal cell fate, lineage and proliferation in the Arabidopsis anther. Development 137:2409–2416

    Article  CAS  Google Scholar 

  • Fox T, DeBruin J, Haug Collet K, Trimnell M, Clapp J, Leonard A, Li B, Scolaro E, Collinson S, Glassman K, Miller M, Schussler J, Dolan D, Liu L, Gho C, Albertsen M, Loussaert D, Shen B (2017) A single point mutation in Ms44 results in dominant male sterility and improves nitrogen use efficiency in maize. Plant Biotechnol J 15:942–952

    Article  CAS  Google Scholar 

  • Han F, Yang C, Fang Z, Yang L, Zhuang M, Lv H et al (2015) Inheritance and InDel markers closely linked to petal color gene (cpc-1) in Brassica oleracea. Mol Breed 35:160

    Article  Google Scholar 

  • Han F, Zhang X, Liu X, Su H, Kong C, Fang Z et al (2017) Comparative analysis of genome wide DNA methylation profiles for the genic male sterile cabbage line 01-20S and its maintainer line. Genes 8:159

    Article  Google Scholar 

  • Hong L, Tang D, Shen Y, Hu Q, Wang K, Li M et al (2012) MIL2 (MICROSPORELESS2) regulates early cell differentiation in the rice anther. New Phytol 196:402–413

    Article  CAS  Google Scholar 

  • Huang J, Zhang T, Linstroth L, Tillman Z, Otegui MS, Owen HA, Zhao D (2016) Control of anther cell differentiation by the small protein ligand TPD1 and its receptor EMS1 in Arabidopsis. PLoS Genet 12:e1006147

    Article  Google Scholar 

  • Ito T, Shinozaki K (2002) The MALE STERILITY1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiol 43:1285–1292

    Article  CAS  Google Scholar 

  • Ji J, Yang L, Fang Z, Zhuang M, Zhang Y, Lv H, Liu Y, Li Z (2017) Recessive male sterility in cabbage (Brassica oleracea var. capitata) caused by loss of function of BoCYP704B1 due to the insertion of a LTR-retrotransposon. Theor Appl Genet 130:1441–1451

    Article  CAS  Google Scholar 

  • Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc Natl Acad Sci USA 105:2220–2225

    Article  CAS  Google Scholar 

  • Jung H, Lee D, Lee J, Park D, Kim YJ, Park WY et al (2015) Intron retention is a widespread mechanism of tumor-suppressor inactivation. Nat Genet 47:1242

    Article  CAS  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  Google Scholar 

  • Kelliher T, Walbot V (2011) Emergence and patterning of the five cell types of the Zea mays anther locule. Dev Biol 350:32–49

    Article  CAS  Google Scholar 

  • Laberge-le Couteulx S, Jung HH, Labauge P, Houtteville JP, Lescoat C, Cecillon M et al (1999) Truncating mutations in CCM1, encoding KRIT1, cause hereditary cavernous angiomas. Nat Genet 23:189

    Article  CAS  Google Scholar 

  • Lewandowska MA (2013) The missing puzzle piece: splicing mutations. Int J Clin Exp Pathol 6:2675

    PubMed  PubMed Central  Google Scholar 

  • Liang J, Ma Y, Wu J, Cheng F, Liu B, Wang X (2017) Map-based cloning of the dominant genic male sterile Ms-cd1 gene in cabbage (Brassica oleracea). Theor Appl Genet 130:71–79

    Article  CAS  Google Scholar 

  • Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IA (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930

    Article  CAS  Google Scholar 

  • Liu X, Han F, Kong C, Fang Z, Yang L, Zhang Y et al (2017) Rapid introgression of the Fusarium wilt resistance gene into an elite cabbage line through the combined application of a microspore culture, genome background analysis, and disease resistance-specific marker assisted foreground selection. Front Plant Sci 8:354

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lou P, Kang J, Zhang G, Bonnema G, Fang Z, Wang X (2007) Transcript profling of a dominant male sterile mutant (Ms-cd1) in cabbage during flower bud development. Plant Sci 172:111–119

    Article  CAS  Google Scholar 

  • Lv H, Yang L, Kang J, Wang Q, Wang X, Fang Z et al (2013) Development of InDel markers linked to Fusarium wilt resistance in cabbage. Mol Breed 32:961–967

    Article  CAS  Google Scholar 

  • Lv H, Fang Z, Yang L, Zhang Y, Wang Q, Liu Y et al (2014) Mapping and analysis of a novel candidate Fusarium wilt resistance gene FOC1 in Brassica oleracea. BMC Genomics 15:1094

    Article  Google Scholar 

  • Lv H, Wang Q, Han F, Liu X, Fang Z, Yang L et al (2017) Genome-wide indel/SSR scanning reveals significant loci associated with excellent agronomic traits of a cabbage (Brassica oleracea) elite parental line ‘01–20’. Sci Rep 7:41696

    Article  CAS  Google Scholar 

  • McCormick S (1993) Male gametophyte development. Plant Cell 5:1265–1275

    Article  Google Scholar 

  • Pelletier G, Primard C, Vedel F, Chetrit P, Remy R, Renard M (1983) Intergeneric cytoplasmic hybridization in Cruciferae by protoplast fusion. Mol Genet Genomics 191:244–250

    Article  CAS  Google Scholar 

  • Perez-Prat E, van Lookeren Campagne MM (2002) Hybrid seed production and the challenge of propagating male-sterile plants. Trends Plant Sci 7:199–203

    Article  CAS  Google Scholar 

  • Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sexual Plant Reprod 11:65–80

    Article  CAS  Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2009) FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 26:1641–1650

    Article  CAS  Google Scholar 

  • Reddy ASN, Marquez Y, Kalyna M, Barta A (2013) Complexity of the alternative splicing landscape in plants. Plant Cell 25:3657–3683

    Article  CAS  Google Scholar 

  • Rogozin IB, Carmel L, Csuros M, Koonin EV (2012) Origin and evolution of spliceosomal introns. Biol Direct 7:11

    Article  CAS  Google Scholar 

  • Ruffio-Chable V, Bellis H, Herve Y (1993) A dominant gene for male sterility in cauliflower (Brassica oleracea var. botrytis): phenotype expression, inheritance, and use in F1 hybrid production. Euphytica 67:9–17

    Article  Google Scholar 

  • Sampson DR (1966) Linkage of genetic male sterility with a seedling marker and its use in producing F1 hybrid seed of Brassica oleracea (cabbage, broccoli, kale, etc.). Can J Plant Sci 46:703

    Article  Google Scholar 

  • Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16(Suppl):S46–S60

    Article  CAS  Google Scholar 

  • Simpson CG, McQuade C, Lyon J, Brown JW (1998) Characterization of exon skipping mutants of the COP1 gene from Arabidopsis. Plant J 15:125–131

    Article  CAS  Google Scholar 

  • Umen JG, Guthrie C (1995) A novel role for a U5 snRNP protein in 3′ splice site selection. Genes Dev 9:855–868

    Article  CAS  Google Scholar 

  • Wang XW, Lou P, Bonnema G, Yang BJ, He HJ, Zhang YG, Fang ZY (2005) Linkage mapping of a dominant male sterility gene Mscd1 in Brassica oleracea. Genome 48:848–854

    Article  CAS  Google Scholar 

  • Wang C, Nan G, Kelliher T, Timofejeva L, Vernoud V, Golubovskaya IN et al (2012) Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 139:2594–2603

    Article  CAS  Google Scholar 

  • Yang S, Xie L, Mao H, San Puah C, Yang W, Jiang L et al (2003) Tapetum determinant1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804

    Article  CAS  Google Scholar 

  • Zhang D, Yang L (2014) Specification of tapetum and microsporocyte cells within the anther. Curr Opin Plant Biol 17:49–55

    Article  CAS  Google Scholar 

  • Zhang D, Wu S, An X, Xie K, Dong Z, Zhou Y, Xu L, Fang W, Liu S, Liu S, Zhu T, Li J, Rao L, Zhao J, Wan X (2018) Construction of a multi-control sterility system for a maize male-sterile line and hybrid seed production based on the ZmMs7 gene encoding a PHD-fnger transcription factor. Plant Biotechnol J 16:459–471

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Key Research and Development Program of China (2017YFD0101804), the Central Public-interest Scientific Institution Basal Research Fund (No. 1610102017013), the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-IVFCAAS) and the earmarked fund for the Modern Agro-Industry Technology Research System, China (nycytx-35-gw01). The work reported here was performed in the Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture, Beijing 100081, China.

Author information

Author notes

  1. Fengqing Han and Kaiwen Yuan have contributed equally to this work.

Authors and Affiliations

  1. Germplasm Innovation in Northwest China, Ministry of Agriculture; College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Fengqing Han & Zhiyuan Fang

  2. Institute of Vegetables and Flowers, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture, Chinese Academy of Agricultural Sciences, #12 Zhong Guan Cun Nandajie Street, Beijing, 100081, China

    Fengqing Han, Kaiwen Yuan, Congcong Kong, Limei Yang, Mu Zhuang, Yangyong Zhang, Zhansheng Li, Yong Wang, Zhiyuan Fang & Honghao Lv

  3. Tianjin Kernel Vegetable Research Institute, Jinjing Road, Xiqing District, Tianjin, 300384, China

    Xiaoli Zhang

Authors
  1. Fengqing Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaiwen Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Congcong Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoli Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Limei Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mu Zhuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yangyong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Zhansheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhiyuan Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Honghao Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhiyuan Fang or Honghao Lv.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest to disclose.

Ethical approval

The authors declare that all experiments comply with the current laws of China.

Additional information

Communicated by Carlos F. Quiros.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Han, F., Yuan, K., Kong, C. et al. Fine mapping and candidate gene identification of the genic male-sterile gene ms3 in cabbage 51S. Theor Appl Genet 131, 2651–2661 (2018). https://doi.org/10.1007/s00122-018-3180-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-018-3180-9

Search

Navigation