Skip to main content
Log in

Analysis of the barley bract suppression gene Trd1

Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

A typical barley (Hordeum vulgare) floret consists of reproductive organs three stamens and a pistil, and non-reproductive organs—lodicules and two floral bracts, abaxial called ‘lemma’ and adaxial ‘palea’. The floret is subtended by two additional bracts called outer or empty glumes. Together these organs form the basic structural unit of the grass inflorescence, a spikelet. There are commonly three spikelets at each rachis (floral stem of the barley spike) node, one central and two lateral spikelets. Rare naturally occurring or induced phenotypic variants that contain a third bract subtending the central spikelets have been described in barley. The gene responsible for this phenotype was called the THIRD OUTER GLUME1 (Trd1). The Trd1 mutants fail to suppress bract growth and as a result produce leaf-like structures that subtend each rachis node in the basal portion of the spike. Also, floral development at the collar is not always suppressed. In rice and maize, recessive mutations in NECK LEAF1 (Nl1) and TASSEL SHEATH1 (Tsh1) genes, respectively, have been shown to be responsible for orthologous phenotypes. Fine mapping of the trd1 phenotype in an F3 recombinant population enabled us to position Trd1 on the long arm of chromosome 1H to a 10 cM region. We anchored this to a conserved syntenic region on rice chromosome Os05 and selected a set of candidate genes for validation by resequencing PCR amplicons from a series of independent mutant alleles. This analysis revealed that a GATA transcription factor, recently proposed to be Trd1, contained mutations in 10 out of 14 independent trd1 mutant alleles that would generate non-functional TRD1 proteins. Together with genetic linkage data, we confirm the identity of Trd1 as the GATA transcription factor ortholog of rice Nl1 and maize Tsh1 genes.

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
Fig. 4

References

  • Anastasio AE, Platt A, Horton M, Grotewold E, Scholl R, Borevitz JO, Nordborg M, Bergelson J (2011) Source verification of misidentified Arabidopsis thaliana accessions. Plant J. doi:10.1111/j.1365-313X.2011.04606.x

    PubMed  Google Scholar 

  • Bossinger G, Rohde W, Lundqvist U, Salamini F (1992) Genetics of barley development: mutant phenotypes and molecular aspects. In: Shewry PR (ed) Barley: genetics, biochemistry, molecular biology and biotechnology. C. A. B. International, Wallingford, pp 231–263

    Google Scholar 

  • Bossolini E, Wicker T, Knobel PA, Keller B (2007) Comparison of orthologous loci from small grass genomes Brachypodium and rice: implications for wheat genomics and grass genome annotation. Plant J 49(4):704–717

    Article  PubMed  CAS  Google Scholar 

  • Briggs S (1992) A suppressor of floral leaf development. Maize Genet Coop News Lett 66:50–51

    Google Scholar 

  • Chuck G, Whipple C, Jackson D, Hake S (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137(8):1243–1250

    Article  PubMed  CAS  Google Scholar 

  • Close T, Bhat P, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson J, Wanamaker S, Bozdag S, Roose M, Moscou M, Chao S, Varshney R, Szucs P, Sato K, Hayes P, Matthews D, Kleinhofs A, Muehlbauer G, DeYoung J, Marshall D, Madishetty K, Fenton R, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10(1):582

    Article  PubMed  Google Scholar 

  • Coen E, Nugent JA (1994) Evolution of flowers and inflorescences. Development (Suppl):107–116

  • Corley SB, Carpenter R, Copsey L, Coen E (2005) Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc Natl Acad Sci 102(14):5068–5073

    Article  PubMed  CAS  Google Scholar 

  • Costa JM, Corey A, Hayes PM, Jobet C, Kleinhofs A et al (2001) Molecular mapping of the Oregon Wolfe Barleys: a phenotypically polymorphic doubled-haploid population. Theor Appl Genet 103:415–424

    Article  CAS  Google Scholar 

  • Druka A, Franckowiak J, Lundqvist U, Bonar N, Alexander J, Houston K, Radovic S, Shahinnia F, Vendramin V, Morgante M, Stein N, Waugh R (2011) Genetic dissection of barley morphology and development. Plant Physiol 155:617–627

    Article  PubMed  CAS  Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2011) Geneious v5.0, Available from http://www.geneious.com

  • Franckowiak JD, Lundqvist U (1997) BGS 202; third outer glume, trd. Barley Genet Newslett 26:207–208

    Google Scholar 

  • Franckowiak JD, Lundqvist U (2002) New and revised barley genetic stock descriptions. Barley Genet Newslett 32:120

    Google Scholar 

  • Franckowiak JD, Lundqvist U (2010a) Descriptions of barley genetic stocks for 2010. Barley Genet Newslett 40:45–177

    Google Scholar 

  • Franckowiak JD, Lundqvist U (2010b) BGS 586; third outer glume. Barley Genet Newslett 40:139–140

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4(1):9

    Google Scholar 

  • Ivanova KV (1937) A new character in barley, “third outer glume”: its inheritance and linkage with the colour of the flowering glumes. Bull Appl Bot Genet Plant Breed (Russia) Series II: 339–353

  • Iwata H, Ninomiya S (2006) AntMap: constructing genetic linkage maps using an ant colony optimization algorithm. Breed Sci 56:371–377

    Article  Google Scholar 

  • Khush GS (1987) List of gene markers maintained in the Rice Genetic Stock Center, IRRI. Rice Genetics Newsletter pp 56–61

  • Kirby EJM, Appleyard M (1987) Cereal development guide. Stoneleigh, Kenilworth, UK, NAC Cereal Unit, p 85

    Google Scholar 

  • Kleinhofs A, Kilian A, Saghai Maroof MA, Biyashev RM, Hayes PM et al (1993) A molecular, isozyme and morphological map of the barley (Hordeum vulgare) genome. Theor Appl Genet 86:705–712

    Article  CAS  Google Scholar 

  • Komatsuda T, Pourkheirandish M, He C, Azhaguvel P, Kanamori H, Perovic D, Stein N, Graner A, Wicker T, Tagiri A, Lundqvist U, Fujimura T, Matsuoka M, Matsumoto T, Yano M (2007) Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc Natl Acad Sci 104:1424–1429

    Article  PubMed  CAS  Google Scholar 

  • Konzak C (1953) The third outer glume character in barley. J Hered 44(3):103–104

    Google Scholar 

  • Li H, Xue D, Gao Z, Yan M, Xu W, Xing Z, Huang D, Qian Q, Xue Y (2009) A putative lipase gene EXTRA GLUME1 regulates both empty-glume fate and spikelet development in rice. Plant J 57(4):593–605

    Article  PubMed  CAS  Google Scholar 

  • Liu L, White MJ, MacRae TH (1999) Transcription factors and their genes in higher plants. Eur J Biochem 262(2):247–257

    Article  PubMed  CAS  Google Scholar 

  • Lundqvist U, Franckowiak JD (2002) BGS 619; third outer glume. Barley Genet Newslett 32:120

    Google Scholar 

  • Lundqvist U, Franckowiak JD, Konishi T (1997) New and revised descriptions of barley genes. Barley Genet Newslett 26:22–43

    Google Scholar 

  • Lundqvist U, Franckowiak JD (2007) BGS 586, Bracteatum-d, bra-d revised. Barley Genet Newslett 37:284

    Google Scholar 

  • Mayer KFX, Martis M, Hedley PE, Šimková H, Liu H, Morris JA, Steuernagel B et al (2011) Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell 23:1249–1263

    Article  PubMed  CAS  Google Scholar 

  • McSteen P, Hake S (2001) Barren inflorescence2 regulates axillary meristem development in the maize inflorescence. Development 128:2881–2891

    PubMed  CAS  Google Scholar 

  • Moragues M, Comadran J, Waugh R, Milne I, Flavell AJ, Russell JR (2010) Effects of ascertainment bias and marker number on estimations of barley diversity from high-throughput SNP genotype data. Theor Appl Genet 120:1525–1534

    Article  PubMed  CAS  Google Scholar 

  • Müller KJ, Romano N, Gerstner O, Garcia-Marotot F, Pozzi C, Salamini F, Rohde W (1995) The barley Hooded mutation caused by a duplication in a homeobox gene intron. Nature 374:727–730

    Article  PubMed  Google Scholar 

  • Nagao S, Takahashi M, Kinoshita T (1963) Present status of rice linkage studies and some intriguing associated problems: genetical studies on rice plant. J Fac Agr Hokkaido Univ 54:29–41

    Google Scholar 

  • Omichinski JG, Clore GM, Schaad O, Felsenfeld G, Trainor C, Appella E, Stahl SJ, Gronenborn AM (1993) NMR structure of a specific DNA complex of Zn-containing DNA binding domain of GATA-1. Science 261(5120):438–446

    Article  PubMed  CAS  Google Scholar 

  • Pozzi C, di Pietro D, Halas G, Roig C, Salamini F (2003) Integration of a barley (Hordeum vulgare) molecular linkage map with the position of genetic loci hosting 29 developmental mutants. Heredity 90:390–396

    Article  PubMed  CAS  Google Scholar 

  • Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134(4):1718–1732

    Article  PubMed  CAS  Google Scholar 

  • Rogozin IB, Pavlov YI (2003) Theoretical analysis of mutation hotspots and their DNA sequence context specificity. Mutat Res 544(1):65–85

    Article  PubMed  CAS  Google Scholar 

  • Schmidt RJ, Ambrose BA (1998) The blooming of grass flower development. Curr Opin Plant Biol 1(1):60–67

    Article  PubMed  CAS  Google Scholar 

  • Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3:771–781

    Article  PubMed  Google Scholar 

  • Takahashi R, Yasuda S (1971) Genetics of earliness and growth habit in barley. In: Proceedings of the 2nd International Barley Genetics Symposium. State University Press, Washington, pp 388–408

  • Tsuchiya (1974) Further results of allelism testing in barley. Barley Genet Newslett 4:82–85

    Google Scholar 

  • Waddington SR, Cartwright PM, Wall PC (1983) A quantitative scale of spike initial and pistal development in barley and wheat. Ann Bot 51:119–130

    Google Scholar 

  • Wang LP, Yin HF, Qian Q, Yang J, Huang CF, Hu XH, Luo D (2009) NECK LEAF 1, a GATA type transcription factor, modulates organogenesis by regulating the expression of multiple regulatory genes during reproductive development in rice. Cell Res 19(5):598–611

    Article  PubMed  CAS  Google Scholar 

  • Whipple CJ, Hall DH, DeBlasio S, Taguchi-Shiobara F, Schmidt RJ, Jackson DP (2010) A conserved mechanism of bract suppression in the grass family. Plant Cell 22(3):565–578

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Bacolla A, Wang G, Vasquez KM (2010) Non-B DNA structure-induced genetic instability and evolution. Cell Mol Life Sci 67(1):43–62

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The work reported in this paper was funded through European Research Area Networks in plant genomics project number ERAPGFP/06.046A - Genomics-Assisted Dissection of Barley Morphology and Development awarded to RW, NS and MM via their respective funding agencies. We would like to thank Harold Bockelman at the National Small Grains Collection, Aberdeen ID USA, David Marshall who combined sequence information from Bowman and Morex NGS assemblies which allowed us to locate the promoter region of Trd1, Sean Chapman and Martin Kierans for help with SEM work, and David Harrap for generating BW069 x Barke F2 seeds.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robbie Waugh.

Additional information

Communicated by T. Close.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2012_1814_MOESM1_ESM.pdf

Online Resource 1. This includes all mutant lines that had previously been described as Trd1. Details of donor line cultivar, backcross stage and mutagen used to generate the line are provided. (PDF 38 kb)

122_2012_1814_MOESM2_ESM.pdf

Online Resource 2. Details of the SNPs used in the 384-SNP Illumina GoldenGate oligo pool assay. The name refers to the SNP id in Close et al. (2009). (PDF 135 kb)

122_2012_1814_MOESM3_ESM.pdf

Online Resource 3. Dendrogram based on bead express analysis of 384 SNPs in all lines included in this study. Where appropriate new nomenclature for the lines has been used, otherwise previous names are given. (PDF 130 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Houston, K., Druka, A., Bonar, N. et al. Analysis of the barley bract suppression gene Trd1 . Theor Appl Genet 125, 33–45 (2012). https://doi.org/10.1007/s00122-012-1814-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-012-1814-x

Keywords

Navigation