Skip to main content
SpringerLink
Log in

Nucleotide sequence variation of GLABRA1 contributing to phenotypic variation of leaf hairiness in Brassicaceae vegetables

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

Abstract

GLABRA1 (GL1) belongs to the group of R2R3-MYB transcription factors and is known to be essential for trichome initiation in Arabidopsis. In our previous study, we identified a GL1 ortholog in Brassica rapa as a candidate for the gene controlling leaf hairiness by QTL analysis and suggested that a 5-bp deletion (B-allele) and a 2-bp deletion (D-allele) in the exon 3 of BrGL1 and a non-synonymous SNP (C-allele) in the second nucleotide of exon 3 possibly cause leaf hairlessness. In this study, we transformed a B. rapa line having the B-allele with the A-allele (wild type) or the C-allele of BrGL1 under the control of the CaMV 35S promoter. The transgenic plants with the A-allele showed dense coverage of seedling tissues including stems, young leaves and hypocotyls with trichomes, whereas the phenotypes of those with the C-allele were unchanged. In order to obtain more information about allelic variation of GL1 in different plant lineages and its correlation with leaf hairiness, two GL1 homologs, i.e., RsGL1a and RsGL1b, in Raphanus sativus were analyzed. Allelic variation of RsGL1a between a hairless line and a hairy line was completely associated with hairiness in their BC1F1 population. Comparison of the full-length of RsGL1a in the hairless and hairy lines showed great variation of nucleotides in the 3′ end, which might be essential for its function and expression.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Esau K (1977) Anatomy of seed plants, 2nd edn. Wiley, New York

    Google Scholar 

  • Esch JJ, Chen M, Sanders M, Hillestad M, Ndkium S, Idelkope B, Neizer J, Marks MD (2003) A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis. Development 130:5885–5894

    Article  PubMed  CAS  Google Scholar 

  • Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    Article  PubMed  CAS  Google Scholar 

  • Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132:1107–1114

    Article  PubMed  CAS  Google Scholar 

  • Grotewold E, Sainz MB, Tagliani L, Hernandez JM, Bowen B, Chandler VL (2000) Identification of the residues in the Myb domain of maize C1 that specify the interaction with the bHLH cofactor R. Proc Natl Acad Sci USA 97:13579–13584

    Article  PubMed  CAS  Google Scholar 

  • Gruber MY, Wang S, Ethier S, Holowachuk J, Bonham-Smith PC, Soroka J, Lloyd A (2006) “HAIRY CANOLA”—Arabidopsis GL3 induces a dense covering of trichomes on Brassica napus seedlings. Plant Mol Biol 60:679–698

    Article  PubMed  CAS  Google Scholar 

  • Hauser MT, Harr B, Schlotterer C (2001) Trichome distribution in Arabidopsis thaliana and its close relative Arabidopsis lyrata: molecular analysis of the candidate gene GLABROUS1. Mol Biol Evol 18:1754–1763

    Article  PubMed  CAS  Google Scholar 

  • Hilscher J, Schlötterer C, Hauser M-T (2009) A single amino acid replacement in ETC2 shapes trichome patterning in natural Arabidopsis populations. Curr Biol 19:1747–1751

    Article  PubMed  CAS  Google Scholar 

  • Hülskamp M (2004) Plant trichomes: a model for cell differentiation. Nat Rev 5:471–480

    Article  Google Scholar 

  • Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S, Okada K, Wada T (2007) Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19:2531–2543

    Article  PubMed  CAS  Google Scholar 

  • Johnson HB (1975) Plant pubescence: an ecological perspective. Bot Rev 41:233–258

    Article  Google Scholar 

  • Johnson CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14:1359–1375

    Article  PubMed  CAS  Google Scholar 

  • Kawagoe T, Shimizu KK, Kakutani T, Kudoh H (2011) Coexistence of trichome variation in a natural plant population: a combined study using ecological and candidate gene approaches. PLoS One 6:e22184

    Article  PubMed  CAS  Google Scholar 

  • Kirik V, Simon M, Wester K, Schiefelbein J, Hülskamp M (2004) ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis. Plant Mol Biol 55:389–398

    Article  PubMed  CAS  Google Scholar 

  • Kivimäki M, Kärkkäinen K, Gaudeul M, Løe G, Ågren J (2007) Gene, phenotype and function: GLABROUS1 and resistance to herbivory in natural populations of Arabidopsis lyrata. Mol Ecol 16:453–462

    Article  PubMed  Google Scholar 

  • Larkin JC, Oppenheimer DG, Pollock S, Marks MD (1993) Arabidopsis GLABROUS1 gene requires downstream sequences for function. Plant Cell 5:1739–1748

    PubMed  CAS  Google Scholar 

  • Li F, Kitashiba H, Inaba K, Nishio T (2009) A Brassica rapa linkage map of EST-based SNP markers for identification of candidate genes controlling flowering time and leaf morphological traits. DNA Res 16:311–323

    Article  PubMed  CAS  Google Scholar 

  • Li F, Kitashiba H, Nishio T (2011) Association of sequence variation in Brassica GLABRA1 orthologs with leaf hairiness. Mol Breeding 28:577–584

    Article  CAS  Google Scholar 

  • Masucci JD, Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, Schiefelbein JW (1996) The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122:1253–1260

    PubMed  CAS  Google Scholar 

  • Mauricio R, Rausher MD (1997) Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51:1435–1444

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Oppenheimer DG, Herman PL, Sivakumaran S, Esch J, Marks MD (1991) A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67:483–493

    Article  PubMed  CAS  Google Scholar 

  • Payne CT, Zhang F, Lloyd AM (2000) GL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1. Genetics 156:1349–1362

    PubMed  CAS  Google Scholar 

  • Pesch M, Hülskamp M (2009) One, two, three models for trichome patterning in Arabidopsis? Curr Opin Plant Biol 12:587–592

    Article  PubMed  CAS  Google Scholar 

  • Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8:1388–1399

    Article  PubMed  CAS  Google Scholar 

  • Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jurgens G, Hülskamp M (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21:5036–5046

    Article  PubMed  CAS  Google Scholar 

  • Shiokai S, Shirasawa K, Sato Y, Nishio T (2010) Improvement of the dot-blot-SNP technique for efficient and cost-effective genotyping. Mol Breeding 25:179–185

    Article  CAS  Google Scholar 

  • Siebert PD, Chenchik A, Kellogg DE, Lukyanov KA, Lukyanov SA (1995) An improved PCR method for walking in uncloned genomic DNA. Nucleic Acids Res 23:1087–1088

    Article  PubMed  CAS  Google Scholar 

  • Symonds VV, Godoy AV, Alconada T, Botto JF, Juenger TE, Casal JJ, Lloyd AM (2005) Mapping quantitative trait loci in multiple populations of Arabidopsis thaliana identifies natural allelic variation for trichome density. Genetics 169:1649–1658

    Article  PubMed  CAS  Google Scholar 

  • Szymanski DB, Lloyd AM, Marks MD (2000) Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis. Trends Plant Sci 5:214–219

    Article  PubMed  CAS  Google Scholar 

  • Takasaki T, Hatakeyama K, Ojima K, Watanabe M, Toriyama K, Hinata K (1997) Factors influencing Agrobacterium-mediated transformation of Brassica rapa L. Breed Sci 47:127–134

    Google Scholar 

  • Uphof JCT (1962) Plant hairs. In: Zimmermann W, Ozenda PG (eds) Encyclopedia of plant anatomy, vol 5(4). Gebruder Borntraeger, Berlin, pp 1–206

    Google Scholar 

  • Wada T, Tachibana T, Shimura Y, Okada K (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277:1113–1116

    Article  PubMed  CAS  Google Scholar 

  • Walker AR, Davison PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundell TL, Esch JJ, Marks MD, Gray JC (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11:1337–1350

    PubMed  CAS  Google Scholar 

  • Wang S, Chen JG (2008) Arabidopsis transient expression analysis reveals that activation of GLABRA2 may require concurrent binding of GLABRA1 and GLABRA3 to the promoter of GLABRA2. Plant Cell Physiol 49:1792–1804

    Article  PubMed  Google Scholar 

  • Wang N, Qian W, Suppanz I, Wei L, Mao B, Long Y, Meng J, Müller AE, Jung C (2011) Flowering time variation in oilseed rape (Brassica napus L.) is associated with allelic variation in the FRIGIDA homologue BnaA.FRI.a. J Exp Bot 62:5641–5658

    Article  PubMed  CAS  Google Scholar 

  • Yuan YX, Wu J, Sun RF, Zhang XW, Xu DH, Bonnema G, Wang XW (2009) A naturally occurring splicing site mutation in the Brassica rapa FLC1 gene is associated with variation in flowering time. J Exp Bot 60:1299–1308

    Article  PubMed  CAS  Google Scholar 

  • Zhang F, Gonzalez A, Zhao M, Payne CT, Lloyd A (2003) A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130:4859–4869

    Article  PubMed  CAS  Google Scholar 

  • Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd A (2008) The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135:1991–1999

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. Ishida of NARO Institute of Vegetable and Tea Science and Dr. Sakamoto of Takii Seed Co. Ltd. for providing plant materials of R. sativus. This work was supported in part by the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN).

Author information

Author notes

  1. Feng Li

    Present address: Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Wuhan, 430062, Hubei Province, China

Authors and Affiliations

  1. Laboratory of Plant Breeding and Genetics, Graduate School of Agricultural Science, Tohoku University, 1-1 Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai, Miyagi, 981-8555, Japan

    Feng Li, Zhongwei Zou, Hui-Yee Yong, Hiroyasu Kitashiba & Takeshi Nishio

Authors
  1. Feng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhongwei Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hui-Yee Yong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hiroyasu Kitashiba
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takeshi Nishio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takeshi Nishio.

Additional information

Communicated by M. Havey.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, F., Zou, Z., Yong, HY. et al. Nucleotide sequence variation of GLABRA1 contributing to phenotypic variation of leaf hairiness in Brassicaceae vegetables. Theor Appl Genet 126, 1227–1236 (2013). https://doi.org/10.1007/s00122-013-2049-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-013-2049-1

Keywords

Search

Navigation